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Telomerase and its extracurricular activities

Cellular & Molecular Biology Letters volume 18, pages 538–554 (2013)Cite this article

Abstract

The classical activity of telomerase is to synthesize telomeric repeats and thus maintain telomere length, which in turn ensures chromosome stability and cellular proliferation. However, there is growing evidence that implicates telomerase in many other functions that are independent of TERC being used as its template. Telomerase has an RNA-dependent RNA polymerase (RdRP) activity in the mitochondria. Other than viral RdRPs, it is the only RNA-dependent RNA polymerase that has been identified in mammals. It also plays a role in the Wnt signaling pathway by acting as a transcriptional modulator. Telomerase acts as a reverse transcriptase independent of its core subunit, TERC. Studies indicate that telomerase is also involved in apoptosis and DNA repair.

Abbreviations

BRG1:

Brahma-related gene 1

PIP1:

POT1-interacting protein 1

PTOP:

POT1- and TIN2-organizing protein

RAP1:

repressor and activator protein 1

RdRP:

RNA-dependent RNA polymerase

SMARCA4:

SWI/SNF-related matrix-associated actin-dependent regulator of chromatin, subfamily a, member 4

SWI/SNF:

SWItch/sucrose non-fermentable

TEP1:

telomerase-associated protein 1

TINT1:

TIN2 Interacting Protein 1

TIN2 or TINF2:

TRF1-interacting nuclear protein 2

TRF1 or TERF1:

telomeric repeat-binding factor 1

TRF2 or TERF2:

telomeric repeat-binding factor 2

References

  1. 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 (1973) 181–190.

    Article  CAS  PubMed  Google Scholar 

  2. Watson, J.D. Origin of concatemeric T7 DNA. Nat. New Biol. 239 (1972) 197–201.

    Article  CAS  PubMed  Google Scholar 

  3. Palm, W. and de Lange, T. How shelterin protects mammalian telomeres. Annu. Rev. Genet. 42 (2008) 301–334.

    Article  CAS  PubMed  Google Scholar 

  4. Liu, D., Safari, A., O’Connor, M., Chan, D.W., Laegeler, A., Qin, J. and Songyang, Z. PTOP interacts with POT1 and regulates its localization to telomeres. Nat. Cell. Biol. 6 (2004) 673–680.

    Article  CAS  PubMed  Google Scholar 

  5. Houghtaling, B.R., Cuttonaro, L., Chang, W. and Smith, S. A dynamic molecular link between the telomere length regulator TRF1 and the chromosome end protector TRF2. Curr. Biol. 14 (2004) 1621–1631.

    Article  CAS  PubMed  Google Scholar 

  6. Ye, J.Z., Hockemeyer, D., Krutchinsky, A.N., Loayza, D., Hooper, S., Chait, B.T. and De Lange, T. POT1-interacting protein PIP1: a telomere length regulator that recruits POT1 to the TIN2/TRF1 complex. Genes Dev. 18 (2004) 1649–1654.

    Article  CAS  PubMed  Google Scholar 

  7. De Lange, T. Shelterin: the protein complex that shapes and safeguards human telomeres. Genes Dev. 19 (2005) 2100–2110.

    Article  PubMed  Google Scholar 

  8. Henderson, E.R and Blackburn, E.H. An overhanging 39 terminus is a conserved feature of telomeres. Mol. Cell. Biol. 9 (1989) 345–348.

    CAS  PubMed Central  PubMed  Google Scholar 

  9. Makarov, V.L., Hirose, Y. and Langmore J.P. Long G tails at both ends of human chromosomes suggest a C strand degradation mechanism for telomere shortening. Cell 88 (1997) 657–666.

    Article  CAS  PubMed  Google Scholar 

  10. McElligott, R. and Wellinger, R.J. The terminal DNA structure of mammalian chromosomes. EMBO J. 16 (1997) 3705–3714.

    Article  CAS  PubMed  Google Scholar 

  11. Woodring, E.W., Valerie. M.T., Kenneth, E.H., Stephen, D.L., and Jerry, W.S. Normal human chromosomes have long G-rich telomeric overhangs at one end. Genes Dev. 11 (1997) 2801–2809.

    Article  Google Scholar 

  12. Greider, C.W. and Blackburn, E.H. Identification of a specific telomere terminal transferase enzyme with two kinds of primer specificity. Cell 51 (1985) 405–413.

    Article  Google Scholar 

  13. 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. Specific association of human telomerase activity with immortal cells and cancer. Science 266 (1994) 2011–2015.

    Article  CAS  PubMed  Google Scholar 

  14. Chang, J.T., Chen, Y.L., Yang, H.T., Chen, C.Y. and Cheng, A.J. Differential regulation of telomerase activity by six telomerase subunits. Eur. J. Biochem. 269 (2002) 3442–3450.

    Article  CAS  PubMed  Google Scholar 

  15. Greider, C.W. and Blackburn, E.H. A telomeric sequence in the RNA of Tetrahymena telomerase required for telomere repeat synthesis. Nature 337 (1989) 331–337.

    Article  CAS  PubMed  Google Scholar 

  16. Blasco, M.A., Funk, W., Villeponteau, B. and Greider, C.W. Functional characterization and developmental regulation of mouse telomerase RNA. Science 269 (1995) 1267–1270.

    Article  CAS  PubMed  Google Scholar 

  17. Feng, J., Funk, WD., Wang. S.S., Weinrich, S.L., Avilion, A.A., Chiu, C.P, Adams R.R, Chang, E., Allsopp, R.C., Yu, J., Le, S., West, M.D., Harley, C.B., Andrews, W.H., Greider, C.W. and Villeponteau, B. The RNA component of human telomerase. Science 269 (1995) 1236–1241.

    Article  CAS  PubMed  Google Scholar 

  18. Chen, J.L. and Greider, C.W. Determinants in mammalian telomerase RNA that mediate enzyme processivity and cross-species incompatibility. EMBO J. 22 (2003) 304–314.

    Article  PubMed  Google Scholar 

  19. Lai, C.K., Miller, M.C. and Collins, K. Roles for RNA in telomerase nucleotide and repeat addition processivity. Mol. Cell. 11 (2003) 1673–1683.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  20. Chen, J.L., Blasco, M.A. and Greider, C.W. Secondary structure of vertebrate telomerase RNA. Cell 100 (2000) 503–514.

    Article  CAS  PubMed  Google Scholar 

  21. Seto, A.G., Umansky, K., Tzfati, Y., Zang, A.J., Blackburn, E.H. and Cech, T.R. A template-proximal RNA paired elements contributes to saccharomyces cerevisiae telomerase activity. RNA 9 (2003) 1323–1332.

    Article  CAS  PubMed  Google Scholar 

  22. Mitchell, J.R., Cheng, J. and Collins, K. A box H/ACA small nucleolar RNA-like domain at the human telomerase RNA 3′ end. Mol. Cell. Biol. 19 (1999) 567–576.

    CAS  PubMed Central  PubMed  Google Scholar 

  23. Chen, J.L., Blasc, M.A. and Greider, C.W. Secondary structure of vertebrate telomerase RNA. Cell 100 (2000) 503–514.

    Article  CAS  PubMed  Google Scholar 

  24. Mitchell, J.R. and Collins, K. Human telomerase activation requires two independent interactions between telomerase RNA and telomerase reverse transcriptase. Mol. Cell. 6 (2000) 361–371.

    Article  CAS  PubMed  Google Scholar 

  25. Matera, A.G., Terns, R.M. and Terns, M.P. Non-coding RNA: lessons from the small nuclear and small nucleolar RNA. Nat. Rev. Mol. Cell. Biol. 8 (2007) 209–220.

    Article  CAS  PubMed  Google Scholar 

  26. Dragon, F., Pogacic. V. and Filipowicz, W. In vitro assembly of human H/ACA small nucleolar ribonucleoproteins reveals unique features of U17 and telomerase RNA. Mol. Cell. Biol. 20 (2000) 3037–3048.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  27. Pogacic, V., Dragon, F. and Filipowicz, W. Human H/ACA small nucleolar ribonucleoproteins and telomerase share evolutionarily conserved proteins NHP2 and NOP10. Mol. Cell. Biol. 20 (2000) 9028–9040.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  28. Zhu, Y., Tomlinson, R.L., Lukowiak, A.A., Terns, R.M. and Terns, M.P. Telomerase RNA accumulates in Cajal bodies in human cancer cells. Mol. Biol. Cell. 15 (2004) 81–90.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  29. Cristofari, G., Adolf, E., Reichenbach, P., Sikora, K., Terns, R.M., Terns, M.P. and Lingner, J. Human telomerase RNA accumulation in Cajal bodies facilitates telomerase recruitment to telomeres and telomere elongation. Mol. Cell. 27 (2007) 882–889.

    Article  CAS  PubMed  Google Scholar 

  30. Zhang, Q., Kim, N.K. and Feigon, J. Architecture of human telomerase RNA. Proc. Natl. Acad. Sci. 108 (2011) 20325–20332.

    Article  CAS  PubMed  Google Scholar 

  31. Lendvay, T.S., Morris, D.K., Sah, J., Balasubramanian, B. and Lundblad, V. Senescence mutants of Sachharomyces cerevisiae with a defect in telomerase replication identify three additional EST genes. Genetics 144 (1996) 1399–1412.

    CAS  PubMed  Google Scholar 

  32. Wick, M., Zubov, D. and Hagen, G. Genomic organization and promoter characterization of the gene encoding the human telomerase reverse transcriptase (hTERT). Gene 232 (1999) 97–106.

    Article  CAS  PubMed  Google Scholar 

  33. Lingner, J., Hughes, T.R., Shevchenko, A., Mann, M., Lundblad, V. and Cech, T.R. Reverse transcriptase motifs in the catalytic subunit of telomerase. Science 276 (1997) 561–567.

    Article  CAS  PubMed  Google Scholar 

  34. Nakamura, T.M., Morin, G.B., Chapman, K.B., Weinrich, S.L., Andrews, W.H., Lingner, J., Harley, C.B. and Cech, T.R. Telomerase catalytic subunit homologs from fission yeast and human. Science 277 (1997) 955–959.

    Article  CAS  PubMed  Google Scholar 

  35. Gillis, A.J., Schuller, A.P. and Skordalakes, E. Structure of the Tribolium castaneum telomerase catalytic subunit TERT. Nature 455 (2008) 633–637.

    Article  CAS  PubMed  Google Scholar 

  36. Mitchell, M., Gillis, A., Futahashi, M., Fujiwara, H. and Skordalakes, E. Structural basis for telomerase catalytic subunit TERT binding to RNA template and telomeric DNA. Nature Struct. Mol. Biol. 17 (2010) 513–518.

    Article  CAS  Google Scholar 

  37. Bodnar, A.G., Ouellette, M., Frolkis, M., Holt, S.E., Chiu, C.P., Morin, G.B., Harley, C.B., Shay, J.W., Lichtsteiner, S. and Wright, W.E. Extension of lifespan by introduction of telomerase in to normal human cells. Science 279 (1998) 349–352.

    Article  CAS  PubMed  Google Scholar 

  38. Cayuela, M.L., Flores, J.M. and Blasco, M.A. The telomerase RNA component Terc is required for the tumour-promoting effects of Tert overexpression. EMBO Rep. 6 (2005) 268–274.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  39. Canela, A., Martin-Caballero, J., Flores, J.M. and Blasco, M.A. Constitutive expression of tert in thymocytes leads to increased incidence and dissemination of T-cell lymphoma in Lck-Tert mice. Mol. Cell. Biol. 24 (2004) 4275–4293.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  40. Engelhardt, M., Drullinsky, P., Guillem, J. and Moore, M.A. Telomerase and telomere length in the development and progression of premalignant lesions to colorectal cancer. Clin. Cancer Res. 3 (1997) 1931–1941.

    CAS  PubMed  Google Scholar 

  41. Hara, E., Tsurui, H., Shinozaki, A., Nakada, S. and Oda, K. Cooperative of antisense-Rb and antisense-p53 oligomers on the extension of lifespan in human diploid fibroblasts, TIG-1 Biochem. Biophys. Res. Commun. 179 (1991) 528–534.

    Article  CAS  PubMed  Google Scholar 

  42. Counter, C.M., Avilion, A.A., LeFeuvre, C.E., Stewart, N.G., Greider, C.W., Harley, C.B. and Bacchetti, S. Telomere shortening associated with chromosome instability is arrested in immortal cells which express telomerase activity. EMBO J. 11 (1992) 1921–1929.

    CAS  PubMed  Google Scholar 

  43. Shay, J.W. and Wright, W.E. Quantitaion of the frequency of immortalization of normal human diploid fibroblasts by sv 40 large T-antigen. Exp. Cell Res. 184 (1989) 109–118.

    Article  CAS  PubMed  Google Scholar 

  44. Zhu, J., Wang, H., Bishop, J.M. and Blackburn, E.H. Telomerase extends the lifespan of virus-transformed human cells without net telomere lengthening. Proc. Natl. Acad. Sci. USA 96 (1999) 3723–3728.

    Article  CAS  PubMed  Google Scholar 

  45. Ding, D., Zhou. J., Wang, M. and Cong, Y. Implications of telomereindependent activities of telomerase reverse transcriptase in human cancer. FEBS J. 280 (2013) 3205–3211.

    Article  CAS  PubMed  Google Scholar 

  46. Kim, M., Xu, L. and Blackburn, E.H. Catalytically active human telomerase mutants with allele-specific biological properties. Exp. Cell. Res. 288 (2003) 277–287.

    Article  CAS  PubMed  Google Scholar 

  47. Kenkichi, M., Possemato, R., Wong, J.M., Currier, J.L., Tothova, Z., Manola, J.B., Ganesan, S., Lansdorp, P.M., Collins, K. and Hahn, W.C. The telomerase reverse transcriptase regulates chromatin state and DNA damage responses. Proc. Natl. Acad. Sci. USA 102 (2005) 8222–8227.

    Article  Google Scholar 

  48. Stampfer, M.R., Garbe, J., Levine, G., Lichtsteiner, S., Vasserot, A.P. and Yaswen, P. Expression of the telomerase catalytic subunit, hTERT, induces resistance to transforming growth factor beta growth inhibition in p16INK4A (−) human mammary epithelial cells. Proc. Natl. Acad. Sci. USA 98 (2001) 4498–4503.

    Article  CAS  PubMed  Google Scholar 

  49. Lindvall, C., Hou, M., Komurasaki, T., Zheng, C., Henriksson, M., Sedivy, J.M., Bjorkholm, M., Teh, B.T., Nordenskjold, M. and Xu, D. Molecular characterization of human telomerase reverse transcriptase-immortalized human fibroblasts by gene expression profiling: activation of the epiregulin gene. Cancer Res. 63 (2003) 1743–1747.

    CAS  PubMed  Google Scholar 

  50. Choi, J., Southworth, L.K., Sarin, K.Y., Venteicher, A.S., Ma, W., Chang, W., Cheung, P., Jun, S., Artandi, M.K., Shah, N., Kim, S.K. and Artandi, S.E. TERT promotes epithelial proliferation through transcriptional control of a Myc- and Wnt related developmental program. PLoS Genet. 4 (2008) e10.

    Article  PubMed Central  PubMed  Google Scholar 

  51. VanMater, D., Kolligs, F.T., Dlugosz, A.A. and Fearon, E.R. Transient activation of beta-catenin signaling in cutaneous keratinocytesis sufficient to trigger the active growth phase of the hair cycle in mice. Genes Dev. 17 (2003) 1219–1224.

    Article  CAS  Google Scholar 

  52. Reya, T. and Clevers, H. Wnt signaling in stem cells and cancer. Nature 434 (2005) 843–850.

    Article  CAS  PubMed  Google Scholar 

  53. Wege, H., Heim, D., Lütgehetmann, M., Dierlamm, J., Lohse, A.W. and Brümmendorf, T.H. Forced activation of β-catenin signaling supports the transformation of hTERT-immortalized human fetal hepatocytes. Mol. Cancer Res. 9 (2011) 1222–1231.

    Article  CAS  PubMed  Google Scholar 

  54. Chiodi, I. and Mondello, C. Telomere-independent function of telomerase in nuclei, cytoplasm, and mitochondria. Front. Oncol. 2 (2012) 1–6.

    Article  Google Scholar 

  55. Rao, T.P. and Ku’hl, M. An updated overview on Wnt signaling pathways: a prelude for more. Circ. Res. 106 (2010) 1798–1806.

    Article  CAS  PubMed  Google Scholar 

  56. Komiya, Y. and Habas, R. Wnt signal transduction pathways. Organogenesis 4 (2008) 68–75.

    Article  PubMed Central  PubMed  Google Scholar 

  57. Barker, N., Hurlstone, A., Musisi, H., Miles, A., Bienz, M. and Clevers, H. The chromatin remodeling factor Brg-1 interacts with beta-catenin to promote target gene activation. EMBO J. 20 (2001) 4935–4943.

    Article  CAS  PubMed  Google Scholar 

  58. Surendran, K. and Simon, T.C. CNP gene expression is activate by Wnt signaling and correlates with Wnt4 expression during renal injury. Am. J. Physiol. Renal Physiol. 284 (2003) F653–F662.

    CAS  PubMed  Google Scholar 

  59. Jho, E., ZhanDomon, C., Joo, C.K., Freund, J.N. and Costantini, F. Wnt/ β — catenin/Tcf signaling induces the transcription of Axin2 a negative regulator of the signaling pathway. Mol. Cell. Biol. 22 (2002) 1172–1183.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  60. Katoh, M and Katoh, M. Integrative genomic analyses of WNT11: Transcriptional mechanisms based on canonical WNT signals and GATA transcription factors. Int. J. Mol. Med. 24 (2009) 247–251.

    Article  CAS  PubMed  Google Scholar 

  61. Park, J.I., Venteicher, A.S., Hong, J.Y., Choi, J., Jun, S., Shkreli, M., Chang, W., Meng, Z., Cheung, P., Ji, H., McLaughlin, M., Veenstra, T.D., Nusse, R., McCrea, P.D. and Artandi S.E. Telomerase modulates Wnt signaling by association with target gene chromatin. Nature 460 (2009) 66–72.

    Article  CAS  PubMed  Google Scholar 

  62. Shkreli, M., Sarin, K.Y., Pech, M.F., Papeta, N., Chang, W., Brockman, S.A., Cheung, P., Lee, E., Kuhner, F., Olson, J.L., Kuo, C.J., Gharavi, A.G., D, Agati, V.D. and Artandi, S.E. Reversible cell-cycle entry in adult kidney podocytes through regulated control of telomerase and Wnt signaling. Nat. Med. 18 (2012) 111–119.

    Article  CAS  Google Scholar 

  63. Hoffmeyer, K., Raggioli, A., Rudloff, S., Anton, R., Hierholzer, A., Valle, I.D., Hein, K., Vogt, R. and Kemler, R. Wnt/beta-catenin signaling regulates telomerase in stem cells and cancer cells. Science 336 (2012) 1549–1554.

    Article  CAS  PubMed  Google Scholar 

  64. Zhang, Y., Toh, L.L., Lau, P. and Wang, P. Telomerase reverse transcriptase (TERT) is an ovel target of Wnt/β-catenin pathway in human cancer. J. Biol. Chem. 287 (2012) 32494–32511.

    Article  CAS  PubMed  Google Scholar 

  65. Maida, Y. and Masutomi, K. RNA-dependent RNA polymerases in RNA silencing. Biol. Chem. 392 (2011) 299–304.

    Article  CAS  PubMed  Google Scholar 

  66. Maida, Y., Yasukawa, M., Furuuchi, M., Lassmann, T., Possemato, R., Okamoto, N., Kasim, V., Hayashizaki, Y., Hahn, W.C. and Masutomi, K. An RNA-dependent RNA polymerase formed by TERT and the RMRP RNA. Nature 461 (2009) 230–235.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  67. Ridanpaa, M., Eenennaam, H., Pelin, K., Chadwick, R., Johnson, C., Yuan, B., Venrooij, W., Pruijn, G., Salmela, R., Rockas, S., Kitie, O.M., Kaitila, I. and Chapelle, A. Mutations in the RNA component of RNase MRP cause a pleiotropic human disease, cartilage-hair hypoplasia. Cell 104 (2001) 195–203.

    Article  CAS  PubMed  Google Scholar 

  68. Mukherjee, S., Firpo, E.J., Wang, Y. and Roberts, J.M. Separation of telomerase functions by reverse genetics. Proc. Natl. Acad. Sci. USA 108 (2011) E1363–E1371.

    Article  CAS  PubMed  Google Scholar 

  69. Santos, J.H., Meyer, J.N., Skorvaga, M., Annab, L.A. and VanHouten, B. Mitochondrial hTERT exacerbates free-radical-mediated mtDNA damage. Aging Cell 3 (2004) 399–411.

    Article  CAS  PubMed  Google Scholar 

  70. Santos, J.H., Meyer, J.N. and Van Houten, B. Mitochondrial localization of telomerase as a determinant for hydrogen peroxide-induced mitochondrial DNA damage and apoptosis. Hum. Mol. Genet. 15 (2006) 1757–1768.

    Article  CAS  PubMed  Google Scholar 

  71. Haendeler, J., Hoffmann, J., Rahman, S., Zeiher, A.M. and Dimmeler, S. Regulation of telomerase activity and anti-apoptotic function by proteinprotein interaction and phosphorylation. FEBS Lett. 536 (2003) 180–186.

    Article  CAS  PubMed  Google Scholar 

  72. Sharma, N.K., Reyes, A., Green, P., Caron, M.J., Bonini, M.G., Gordon, D.M., Holt, I.J. and Santos, J.H. Human telomerase acts as a hTRindependent reverse transcriptase in mitochondria. Nucleic Acids Res. 40 (2012) 712–725.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  73. Haendeler, J., Hoffmann, J., Diehl, J.F., Vasa, M., Spyridopoulos, I., Zeiher, A.M. and Dimmeler, S. Antioxidants inhibit nuclear export of telomerase reverse transcriptase and delay replicative senescence of endothelial cells. Circ. Res. 94 (2004) 768–775.

    Article  CAS  PubMed  Google Scholar 

  74. Zhang, P., Chan, S.L., Fu, W., Mendoza, M. and Mattson, M.P. TERT suppresses apoptotis at a premitochondrial step by a mechanism requiring reverse transcriptase activity and 14-3-3 protein-binding ability. FASEB J.17 (2003) 767–769.

    CAS  PubMed  Google Scholar 

  75. Massard, C., Zermati, Y., Pauleau, A.L., Larochette, N., Metivier, D., Sabatier, L., Kroemer, G. and Soria, J.C. hTERT: a novel endogenous inhibitor of the mitochondrial cell death pathway. Oncogene 25 (2006) 4505–4514.

    Article  CAS  PubMed  Google Scholar 

  76. Lee, J., Sung., Y.H., Cheong, C., Choi, Y.S., Jeon, H.K., Sun, W., Hahn, W.C., Ishikawa, F., and Lee, H.W. TERT promotes cellular and organismal survival independently of telomerase activity. Oncogene 27 (2008) 3754–3760.

    Article  CAS  PubMed  Google Scholar 

  77. Ray, S., Karamysheva, Z., Wang, L., Shippen, D.E. and Price, C.M. Interactions between telomerase and primase physically link the telomere and chromosome replication machinery. Mol. Cell. Biol. 22 (2002) 5859–5868.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  78. Sharma, G.G., Gupta, A., Wang, H., Scherthan, H., Dhar, S., Gandhi, V., Iliakis, G., Shay, J.W., Young, C.S. and Pandita, T.K. hTERT associates with human telomeres and enhances genomic stability and DNA repair. Oncogene 22 (2003) 131–146.

    Article  CAS  PubMed  Google Scholar 

  79. Sharma, G.G., Hwang, K.K., Pandita, R.K., Gupta, A., Dhar, S., Parenteau, J., Agarwal, M., Worman, H.J. and Wellinger R.J. Human heterochromatin protein 1 isoforms HP1 (Hsalpha) and HP1 (Hsbeta) interfere with hTERTtelomere interactions and correlate with changes in cell growth and response to ionizing radiation. Mol. Cell. Biol. 23 (2003) 8363–8376.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  80. Shin, K.H., Kang, M.K., Dicterow, E., Kameta, A., Baluda, M.A. and Park, N.H. Introduction of human telomerase reverse transcriptase to normal human fibroblasts enhances DNA repair capacity. Clin. Cancer Res. 10 (2004) 2551–2560.

    Article  CAS  PubMed  Google Scholar 

  81. Smith, L.L., Coller, H.A. and Roberts, J.M. Telomerase modulates expression of growth-controlling genes and enhances cell proliferation. Nat. Cell. Biol. 5 (2003) 474–479.

    Article  CAS  PubMed  Google Scholar 

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  1. Applied Molecular Biology Laboratory, School of Life Sciences, Jawaharlal Nehru University, New Delhi, 110067, India

    Rishi Kumar Jaiswal, Pramod Kumar & Pramod Kumar Yadava

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Jaiswal, R.K., Kumar, P. & Yadava, P.K. Telomerase and its extracurricular activities. Cell Mol Biol Lett 18, 538–554 (2013). https://doi.org/10.2478/s11658-013-0105-0

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