A translocation-defective telomerase with low levels of activity and processivity stabilizes short telomeres and confers immortalization

Molecular Biology of the Cell

Volumn 24, Issue 9, 2013, Pages 1469-1479

  D'Souza, Yasmin ^a   Chu, Tsz Wai ^a,b   Autexier, Chantal ^a,b  

^a MCGILL UNIVERSITY   (Canada)

^b MCGILL UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; RNA; TELOMERASE; TELOMERASE REVERSE TRANSCRIPTASE;

APOPTOSIS; ARTICLE; CELL FUNCTION; CELL IMMORTALIZATION; CELL SURVIVAL; CONTROLLED STUDY; DNA SYNTHESIS; ENZYME ACTIVITY; GENE EXPRESSION; HUMAN; HUMAN CELL; IN VITRO STUDY; PRIORITY JOURNAL; PROTEIN DOMAIN; RNA TRANSPORT; TELOMERE; WILD TYPE;

AMINO ACID SEQUENCE; ANIMALS; APOPTOSIS; CELL-FREE SYSTEM; DNA; HEK293 CELLS; HUMANS; MOLECULAR SEQUENCE DATA; MUTATION, MISSENSE; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; RABBITS; TELOMERASE; TELOMERE; TELOMERE HOMEOSTASIS; TRANSLOCATION, GENETIC;

EID: 84877108478     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E12-12-0889     Document Type: Article

References (79)

1. Abreu E, Aritonovska E, Reichenbach P, Cristofari G, Culp B, Terns RM, Lingner J, Terns MP (2010). TIN2-tethered TPP1 recruits human telom-erase to telomeres in vivo. Mol Cell Biol 30, 2971-2982.
2. Abreu E, Terns RM, Terns MP (2011). Visualization of human telomerase localization by fluorescence microscopy techniques. Methods Mol Biol 735, 125-137.
3. Alder JK, Cogan JD, Brown AF, Anderson CJ, Lawson WE, Lansdorp PM, Phillips JA 3rd, Loyd JE, Chen JJ, Armanios M (2011). Ancestral mutation in telomerase causes defects in repeat addition processivity and manifests as familial pulmonary fibrosis. PLoS Genet 7, e1001352.
4. Armanios M, Blackburn EH (2012). The telomere syndromes. Nat Rev Genet 13, 693-704.
5. Armbruster BN, Banik SSR, Guo C, Smith AC, Counter CM (2001). N-terminal domains of the human telomerase catalytic subunit required for enzyme activity in vivo. Mol Cell Biol 21, 7775-7786.
6. Autexier C, Lue N (2006). The structure and function of telomerase reverse transcriptase. Annu Rev Biochem 75, 493-517.
7. Bachand F, Autexier C (1999). Functional reconstitution of human te-lomerase expressed in Saccharomyces cerevisiae. J Biol Chem 274, 38027-38031.
8. Baird DM, Rowson J, Wynford-Thomas D, Kipling D (2003). Extensive allelic variation and ultrashort telomeres in senescent human cells. Nat Genet 33, 203-207.
9. Berman AJ, Akiyama BM, Stone MD, Cech TR (2011). The RNA accordion model for template positioning by telomerase RNA during telomeric DNA synthesis. Nat Struct Mol Biol 18, 1371-1375.
10. Blackburn EH (2001). Switching and signaling at the telomere. Cell 106, 661-673.
11. Brault ME, D'Souza Y, Autexier C (2008). Telomerase: evolution, structure and function. In: Origin and Evolution of Telomeres, ed. J Nosef and L Tomaska, Austin, TX: Landes Bioscience.
12. Britt-Compton B, Capper R, Rowson J, Baird DM (2009). Short telomeres are preferentially elongated by telomerase in human cells. FEBS Lett 583, 3076-3080.
13. Broccoli D, Young JW, de Lange T (1995). Telomerase activity in normal and malignant hematopoietic cells. Proc Natl Acad Sci USA 92, 9082-9086.
14. Cesare AJ, Griffith JD (2004). Telomeric DNA in ALT cells is characterized by free telomeric circles and heterogeneous t-loops. Mol Cell Biol 24, 9948-9957.
15. Cohn M, Blackburn EH (1995). Telomerase in yeast. Science 269, 396-400.
16. Counter CM, Avilion AA, LeFeuvre CE, Stewart NG, Greider CW, Harley CB, Bacchetti S (1992). Telomere shortening associated with chromosome instability is arrested in immortal cells which express telomerase activity. EMBO J 11, 1921-1929.
17. Counter CM, Botelho FM, Wang P, Harley CB, Bacchetti S (1994). Stabilization of short telomeres and telomerase activity accompany immortalization of Epstein-Barr virus-transformed human B lymphocytes. J Virol 68, 3410-3414.
18. Counter CM, Hahn WC, Wei W, Caddle SD, Beijersbergen RL, Lansdorp PM, Sedivy JM, Weinberg RA (1998). Dissociation among in vitro telom-erase activity, telomere maintenance, and cellular immortalization. Proc Natl Acad Sci USA 95, 14723-14728.
19. Counter CM, Meyerson M, Eaton EN, Weinberg RA (1997). The catalytic subunit of yeast telomerase. Proc Natl Acad Sci USA 94, 9202-9207.
20. Cristofari G, Adolf E, Reichenbach P, Sikora K, Terns RM, Terns M P, Lingner J (2007). Human telomerase RNA accumulation in Cajal bodies facilitates telomerase recruitment to telomeres and telomere elongation. Mol Cell 27, 882-889.
21. Cristofari G, Lingner J (2006). Telomere length homeostasis requires that telomerase levels are limiting. EMBO J 25, 565-574.
22. D'Souza Y, Lauzon C, Chu TW, Autexier C (2013). Regulation of telomere length and homeostasis by telomerase enzyme processivity. J Cell Sci 126, 676-687.
23. Damm K et al. (2001). A highly selective telomerase inhibitor limiting human cancer cell proliferation. EMBO J 20, 6958-6968.
24. de Lange T (2005). Shelterin: the protein complex that shapes and safeguards human telomeres. Genes Dev 19, 2100-2110.
25. Gillis AJ, Schuller A P, Skordalakes E (2008). Structure of the Tribolium casta-neum telomerase catalytic subunit TERT. Nature 455, 633-637.
26. Greider CW (1991). Telomerase is processive. Mol Cell Biol 11, 4572-4580.
27. Greider CW, Blackburn EH (1987). The telomere terminal transferase of Tetrahymena is a ribonucleoprotein enzyme with two kinds of primer specificity. Cell 51, 887-898.
28. Griffith JD, Comeau L, Rosenfield S, Stansel RM, Bianchi A, Moss H, de Lange T (1999). Mammalian telomeres end in a large duplex loop. Cell 97, 503-514.
29. Hamad NM, Banik SS, Counter CM (2002). Mutational analysis defines a minimum level of telomerase activity required for tumourigenic growth of human cells. Oncogene 21, 7121-7125.
30. Hardy CD, Schultz CS, Collins K (2001). Requirements for the dGTP-dependent repeat addition processivity of recombinant Tetrahymena telomerase. J Biol Chem 276, 4863-4871.
31. Harley CB, Futcher AB, Greider CW (1990). Telomeres shorten during ageing of human fibroblasts. Nature 345, 458-460.
32. Harrington L, Zhou W, McPhail T, Oulton R, Yeung DSK, Mar V, Bass MB, Robinson MO (1997). Human telomerase contains evolutionarily conserved catalytic and structural subunits. Genes Dev 11, 3109-3115.
33. Hemann MT, Strong MA, Hao L-Y, Greider CW (2001). The shortest telom-ere, not average telomere length, is critical for cell viability and chromosome stability. Cell 107, 67-77.
34. Huard S, Moriarty TJ, Autexier C (2003). The C terminus of the human te-lomerase reverse transcriptase is a determinant of enzyme processivity. Nucleic Acids Res 31, 4059-4070.
35. Jacobs SA, Podell ER, Cech TR (2006). Crystal structure of the essential N-terminal domain of telomerase reverse transcriptase. Nat Struct Mol Biol 13, 218-225.
36. Jady BE, Richard P, Bertrand E, Kiss T (2006). Cell cycle-dependent recruitment of telomerase RNA and Cajal bodies to human telomeres. Mol Biol Cell 17, 944-954.
37. Ji H, Platts MH, Dharamsi LM, Friedman KL (2005). Regulation of telomere length by an N-terminal region of the yeast telomerase reverse tran-scriptase. Mol Cell Biol 25, 9103-9114.
38. Jurczyluk J, Nouwens AS, Holien JK, Adams TE, Lovrecz GO, Parker MW, Cohen SB, Bryan TM (2011). Direct involvement of the TEN domain at the active site of human telomerase. Nucleic Acids Res 39, 1774-1788.
39. Kim NW, Piatyszek MA, Prowse KR, Harley CB, West MD, Ho PLC, Coviello GM, Wright WE, Weinrich SL, Shay JW (1994). Specific association of human telomerase activity with immortal cells and cancer. Science 266, 2011-2015.
40. Klingelhutz AJ, Barber SA, Smith P P, Dyer K, McDougall JK (1994). Restoration of telomeres in human papillomavirus-immortalized human anogenital epithelial cells. Mol Cell Biol 14, 961-969.
41. Kolquist KA, Ellisen LW, Counter CM, Meyerson M, Tan LK, Weinberg RA, Haber DA, Gerald WL (1998). Expression of TERT in early premalig-nant lesions and a subset of cells in normal tissues. Nature Genet 19, 182-186.
42. Latrick CM, Cech TR (2010). POT1-TPP1 enhances telomerase processivity by slowing primer dissociation and aiding translocation. EMBO J 29, 924-933.
43. Lingner J, Hughes TR, Shevchenko A, Mann M, Lundblad V, Cech TR (1997). Reverse transcriptase motifs in the catalytic subunit of telomerase. Science 276, 561-567.
44. Liu Y, Kha H, Ungrin M, Robinson MO, Harrington L (2002). Preferential maintenance of critically short telomeres in mammalian cells heterozygous for mTert. Proc Natl Acad Sci USA 99, 3597-3602.
45. Lue N (2004). Adding to the ends: what makes telomerase processive and how important is it? BioEssays 26, 955-962.
46. Lue NF, Lin YC, Mian IS (2003). A conserved telomerase motif within the catalytic domain of telomerase reverse transcriptase is specifically required for repeat addition processivity. Mol Cell Biol 23, 8440-8449.
47. Lue NF, Peng Y (1998). Negative regulation of yeast telomerase activity through an interaction with an upstream region of the DNA primer. Nucleic Acids Res 26, 1487-1494.
48. Lundblad V, Szostak JW (1989). A mutant with a defect in telomere elongation leads to senescence in yeast. Cell 57, 633-643.
49. Masutomi K et al. (2003). Telomerase maintains telomere structure in normal human cells. Cell 114, 241-253.
50. Meyerson M et al. (1997). hEST2, the putative human telomerase catalytic subunit gene, is up-regulated in tumor cells and during immortalization. Cell 90, 785-795.
51. Mitchell M, Gillis A, Futahashi M, Fujiwara H, Skordalakes E (2010). Structural basis for telomerase catalytic subunit TERT binding to RNA template and telomeric DNA. Nat Struct Mol Biol 17, 513-518.
52. Moriarty TJ, Marie-Egyptienne DT, Autexier C (2004). Functional organization of repeat addition processivity and DNA synthesis determinants in the human telomerase multimer. Mol Cell Biol 24, 3720-3733.
53. Moriarty TJ, Marie-Egyptienne DT, Autexier C (2005a). Regulation of 5' template usage and incorporation of noncognate nucleotides by human telomerase. RNA 11, 1448-1460.
54. Moriarty TJ, Ward R, Taboski MAS, Autexier C (2005b). An anchor site type defect in human telomerase that disrupts telomere length maintenance and cellular immortalization. Mol Biol Cell 16, 3152-3161.
55. Morin GB (1989). The human telomere terminal transferase enzyme is a ribonucleoprotein that synthesizes TTAGGG repeats. Cell 59, 521-529.
56. Moyzis RK, Buckingham JM, Cram LS, Dani M, Deaven LL, Jones MD, Meyne J, Ratliff RL, Wu J-R (1988). A highly conserved repetitive DNA sequence, (TTAGGG)n, present at the telomeres of human chromosomes. Proc Natl Acad Sci USA 85, 6622-6626.
57. Nakamura TM, Morin GB, Chapman KB, Weinrich SL, Andrews WH, Lingner J, Harley CB, Cech TR (1997). Telomerase catalytic subunit homologs from fission yeast and human. Science 277, 955-959.
58. Olovnikov AM (1973). A theory of marginotomy. J Theor Biol 41, 181-190.
59. Ouellette MM, Liao M, Herbert BS, Johnson M, Holt SE, Liss HS, Shay JW, Wright WE (2000). Subsenescent telomere lengths in fibroblasts immortalized by limiting amounts of telomerase. J Biol Chem 275, 10072-10076.
60. Pascolo E, Wenz C, Lingner J, Hauel N, Priepke H, Kauffmann I, Garin-Chesa P, Rettig WJ, Damm K, Schnapp A (2002). Mechanism of human telomerase inhibition by BIBR1532, a synthetic, non-nucleosidic drug candidate. J Biol Chem 277, 15566-15572.
61. Peng Y, Mian SI, Lue NF (2001). Analysis of telomerase processivity: mechanistic similarity to HIV-1 reverse transcriptase and role in telomere maintenance. Mol Cell 7, 1201-1211.
62. Prescott J, Blackburn EH (1997). Telomerase RNA mutations in Saccharomy-ces cerevisiae alter telomerase action and reveal nonprocessivity in vivo and in vitro. Gene Dev 11, 528-540.
63. Qi X, Xie M, Brown AF, Bley CJ, Podlevsky JD, Chen JJ (2011). RNA/DNA hybrid binding affinity determines telomerase template-translocation efficiency. EMBO J 31, 150-161.
64. Romi E, Baran N, Gantman M, Shmoish M, Min B, Collins K, Manor H (2007). High-resolution physical and functional mapping of the template adjacent DNA binding site in catalytically active telomerase. Proc Natl Acad Sci USA 104, 8791-8796.
65. -/- mice with short telomeres. EMBO Rep 2, 800-807.
66. Shay JW, Wright WE, Brasiskyte D, Van der Haegen BA (1993). E6 of human papilloma type 16 can overcome the M1 stage of immortalization in human mammary epithelial cells but not in human fibroblasts. Oncogene 8, 1407-1413.
67. Stern JL, Zyner KG, Pickett HA, Cohen SB, Bryan TM (2012). Telomerase recruitment requires both TCAB1 and Cajal bodies independently. Mol Cell Biol 32, 2384-2395.
68. Stewart N, Bacchetti S (1991). Expression of SV40 large T antigen, but not small t antigen, is required for the induction of chromosomal aberrations in transformed human cells. Virology 180, 49-57.
69. Tomlinson RL, Abreu EB, Ziegler T, Ly H, Counter CM, Terns RM, Terns MP (2008). Telomerase reverse transcriptase is required for the localization of telomerase RNA to Cajal bodies and telomeres in human cancer cells. Mol Biol Cell 19, 3793-3800.
70. Tomlinson RL, Ziegler TD, Supakorndej T, Terns RM, Terns MP (2006). Cell cycle-regulated trafficking of human telomerase to telomeres. Mol Biol Cell 17, 955-965.
71. Wallweber G, Gryaznov S, Pongracz K, Pruzan R (2003). Interaction of human telomerase with its primer substrate. Biochemistry 42, 589-600.
72. Watson JD (1972). Origin of concatameric T7 DNA. Nat New Biol 239, 197-201.
73. Wright WE, Piatyszek MA, Rainey WE, Byrd W, Shay JW (1996). Telomerase activity in human germline and embryonic tissues and cells. Dev Genet 18, 173-179.
74. Wright WE, Tesmer VM, Huffman KE, Levene SD, Shay JW (1997). Normal human chromosomes have long G-rich telomeric overhangs at one end. Genes Dev 11, 2801-2809.
75. Wyatt HDM, Lobb DA, Beattie TL (2007). Characterization of physical and functional anchor site interactions in human telomerase. Mol Cell Biol 27, 3226-3240.
76. Xie M, Podlevsky JD, Qi X, Bley CJ, Chen JJ (2010). A novel motif in telom-erase reverse transcriptase regulates telomere repeat addition rate and processivity. Nucleic Acids Res 38, 1982-1996.
77. Zhao Y, Abreu E, Kim J, Stadler G, Eskiocak U, Terns M P, Terns RM, Shay JW, Wright WE (2011). Processive and distributive extension of human telomeres by telomerase under homeostatic and nonequilibrium conditions. Mol Cell 42, 297-307.
78. Zhao Y, Sfeir AJ, Zou Y, Buseman CM, Chow TT, Shay JW, Wright WE (2009). Telomere extension occurs at most chromosome ends and is uncoupled from fill-in in human cancer cells. Cell 138, 463-475.
79. Zhong FL, Batista LF, Freund A, Pech MF, Venteicher AS, Artandi SE (2012). TPP1 OB-fold domain controls telomere maintenance by recruiting telomerase to chromosome ends. Cell 150, 481-494.