An alternative telomerase RNA in arabidopsis modulates enzyme activity in response to DNA damage

Genes and Development

Volumn 26, Issue 22, 2012, Pages 2512-2523

  Cifuentes Rojas, Catherine ^a,b   Nelson, Andrew D L ^a,c   Boltz, Kara A ^a   Kannan, Kalpana ^a,d   She, Xintao ^a   Shippen, Dorothy E ^a  

^a TEXAS A AND M UNIVERSITY   (United States)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

^c UNIVERSITY OF ARIZONA   (United States)

^d BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

Noncoding RNA; POT1; Ribonucleoprotein; Telomere; TRAP assay

Indexed keywords

PHLEOMYCIN; RIBONUCLEOPROTEIN; RNA; TELOMERASE; TER2 PROTEIN; UNCLASSIFIED DRUG;

ARABIDOPSIS; ARTICLE; CONTROLLED STUDY; DNA DAMAGE; DOUBLE STRANDED DNA BREAK; ENZYME ACTIVITY; GENE OVEREXPRESSION; IMMUNOPRECIPITATION; IN VITRO STUDY; IN VIVO STUDY; NONHUMAN; PLANT DEVELOPMENT; PLANT GROWTH; PRIORITY JOURNAL; PROTEIN RNA BINDING; TELOMERE;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; DNA DAMAGE; ENZYME ACTIVATION; GENE EXPRESSION REGULATION, PLANT; RIBONUCLEOPROTEINS; RNA; RNA 3' END PROCESSING; RNA SPLICING; TELOMERASE; TELOMERE;

ARABIDOPSIS; ARABIDOPSIS THALIANA;

EID: 84869193935     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.202960.112     Document Type: Article

References (61)

1. Adachi S, Minamisawa K, Okushima Y, Inagaki S, Yoshiyama K, Kondou Y, Kaminuma E, Kawashima M, Toyoda T, Matsui M, et al. 2011. Programmed induction of endoreduplication by DNA double-strand breaks in Arabidopsis. Proc Natl Acad Sci 108: 10004-10009.
2. Adelmant G, Calkins AS, Garg BK, Card JD, Askenazi M, Miron A, Sobhian B, Zhang Y, Nakatani Y, Silver PA, et al. 2012. DNA ends alter the molecular composition and localization of ku multicomponent complexes. Mol Cell Proteomics 11: 411-421.
3. Artandi SE, DePinho RA. 2010. Telomeres and telomerase in cancer. Carcinogenesis 31: 9-18.
4. Balestrazzi A, Confalonieri M, Macovei A, Dona M, Carbonera D. 2011. Genotoxic stress and DNA repair in plants: Emerging functions and tools for improving crop productivity. Plant Cell Rep 30: 287-295.
5. Baumann P, Price C. 2010. Pot1 and telomere maintenance. FEBS Lett 584: 3779-3784.
6. Beilstein MA, Brinegar AE, Shippen DE. 2012. Evolution of the Arabidopsis telomerase RNA. Front Genet 3: 188. doi:10.3389/fncom.04.2012.
7. Boltz KA, Leehy K, Song X, Nelson AD, Shippen DE. 2012. ATR cooperates with CTC1 and STN1 to maintain telomeres and genome integrity in Arabidopsis. Mol Biol Cell 23: 1558-1568.
8. Boule JB, Vega LR, Zakian VA. 2005. The yeast Pif1p helicase removes telomerase from telomeric DNA. Nature 438: 57-61.
9. Boulton SJ, Jackson SP. 1998. Components of the Ku-dependent non-homologous end-joining pathway are involved in telomeric length maintenance and telomeric silencing. EMBO J 17: 1819-1828.
10. Box JA, Bunch JT, Zappulla DC, Glynn EF, Baumann P. 2008. A flexible template boundary element in the RNA subunit of fission yeast telomerase. J Biol Chem 283: 24224-24233.
11. Cao Y, Li H, Deb S, Liu JP. 2002. TERT regulates cell survival independent of telomerase enzymatic activity. Oncogene 21: 3130-3138.
12. Caslini C, Connelly JA, Serna A, Broccoli D, Hess JL. 2009. MLL associates with telomeres and regulates telomeric repeatcontaining RNA transcription. Mol Cell Biol 29: 4519-4526.
13. Chan SW, Blackburn EH. 2003. Telomerase and ATM/Tel1p protect telomeres from nonhomologous end joining. Mol Cell 11: 1379-1387.
14. Cifuentes-Rojas C, Shippen DE. 2012. Telomerase regulation. Mutat Res 730: 20-27.
15. Cifuentes-Rojas C, Kannan K, Tseng L, Shippen DE. 2011. Two RNA subunits and POT1a are components of Arabidopsis telomerase. Proc Natl Acad Sci 108: 73-78.
16. Cohen SB, Graham ME, Lovrecz GO, Bache N, Robinson PJ, Reddel RR. 2007. Protein composition of catalytically active human telomerase from immortal cells. Science 315: 1850-1853.
17. Culligan K, Tissier A, Britt A. 2004. ATR regulates a G2-phase cell cycle checkpoint in Arabidopsis thaliana. Plant Cell 16: 1091-1104.
18. Egan ED, Collins K. 2012. Biogenesis of telomerase ribonucleoproteins. RNA 18: 1747-1759.
19. Evans SK, Lundblad V. 1999. Est1 and Cdc13 as comediators of telomerase access. Science 286: 117-120.
20. Fitzgerald MS, Riha K, Gao F, Ren S, McKnight TD, Shippen DE. 1999. Disruption of the telomerase catalytic subunit gene from Arabidopsis inactivates telomerase and leads to a slow loss of telomeric DNA. Proc Natl Acad Sci 96: 14813-14818.
21. Flint J, Craddock CF, Villegas A, Bentley DP, Williams HJ, Galanello R, Cao A, Wood WG, Ayyub H, Higgs DR. 1994. Healing of broken human chromosomes by the addition of telomeric repeats. Am J Hum Genet 55: 505-512.
22. Fulcher N, Sablowski R. 2009. Hypersensitivity to DNA damage in plant stem cell niches. Proc Natl Acad Sci 106: 20984-20988.
23. Furukawa T, Curtis MJ, Tominey CM, Duong YH, Wilcox BW, Aggoune D, Hays JB, Britt AB. 2010. A shared DNA-damageresponse pathway for induction of stem-cell death by UVB and g irradiation. DNA Repair (Amst) 9: 940-948.
24. Hanish JP, Yanowitz JL, de Lange T. 1994. Stringent sequence requirements for the formation of human telomeres. Proc Natl Acad Sci 91: 8861-8865.
25. Heacock ML, Idol RA, Friesner JD, Britt AB, Shippen DE. 2007. Telomere dynamics and fusion of critically shortened telomeres in plants lacking DNA ligase IV. Nucleic Acids Res 35: 6490-6500.
26. Hsu M, McEachern MJ, Dandjinou AT, Tzfati Y, Orr E, Blackburn EH, Lue NF. 2007. Telomerase core components protect Candida telomeres from aberrant overhang accumulation. Proc Natl Acad Sci 104: 11682-11687.
27. Hu H, Gatti RA. 2011. MicroRNAs: New players in the DNA damage response. J Mol Cell Biol 3: 151-158.
28. Kannan K, Nelson AD, Shippen DE. 2008. Dyskerin is a component of the Arabidopsis telomerase RNP required for telomere maintenance. Mol Cell Biol 28: 2332-2341.
29. Karamysheva Z, Wang L, Shrode T, Bednenko J, Hurley LA, Shippen DE. 2003. Developmentally programmed gene elimination in Euplotes crassus facilitates a switch in the telomerase catalytic subunit. Cell 113: 565-576.
30. Karamysheva ZN, Surovtseva YV, Vespa L, Shakirov EV, Shippen DE. 2004. A C-terminalMyb extension domain defines a novel family of double-strand telomeric DNA-binding proteins in Arabidopsis. J Biol Chem 279: 47799-47807.
31. Kazda A, Zellinger B, Rossler M, Derboven E, Kusenda B, Riha K. 2012. Chromosome end protection by blunt-ended telomeres. Genes Dev 26: 1703-1713.
32. Kharbanda S, Kumar V, Dhar S, Pandey P, Chen C, Majumder P, Yuan ZM, Whang Y, Strauss W, Pandita TK, et al. 2000. Regulation of the hTERT telomerase catalytic subunit by the c-Abl tyrosine kinase. Curr Biol 10: 568-575.
33. Leonardi J, Box JA, Bunch JT, Baumann P. 2008. TER1, the RNA subunit of fission yeast telomerase. Nat Struct Mol Biol 15: 26-33.
34. Linger BR, Price CM. 2009. Conservation of telomere protein complexes: Shuffling through evolution. Crit Rev Biochem Mol Biol 44: 434-446.
35. Lu C, Meyers BC, Green PJ. 2007. Construction of small RNA cDNA libraries for deep sequencing. Methods 43: 110-117.
36. Luke B, Lingner J. 2009. TERRA: Telomeric repeat-containing RNA. EMBO J 28: 2503-2510.
37. Makovets S, Blackburn EH. 2009. DNA damage signaling prevents deleterious telomere addition at DNA breaks. Nat Cell Biol 11: 1383-1386.
38. Menges M, Murray JA. 2002. Synchronous Arabidopsis suspension cultures for analysis of cell cycle gene activity. Plant J 30: 203-212.
39. Mitchell JR, Collins K. 2000. Human telomerase activation requires two independent interactions between telomerase RNA and telomerase reverse transcriptase. Mol Cell 6: 361-371.
40. Pennock E, Buckley K, Lundblad V. 2001. Cdc13 delivers separate complexes to the telomere for end protection and replication. Cell 104: 387-396.
41. Pfingsten JS, Goodrich KJ, Taabazuing C, Ouenzar F, Chartrand P, Cech TR. 2012. Mutually exclusive binding of telomerase RNA and DNA by Ku alters telomerase recruitment model. Cell 148: 922-932.
42. Ponting CP, Oliver PL, Reik W. 2009. Evolution and functions of long noncoding RNAs. Cell 136: 629-641.
43. Ren S, Johnston JS, Shippen DE, McKnight TD. 2004. TELOMERASE ACTIVATOR1 induces telomerase activity and potentiates responses to auxin in Arabidopsis. Plant Cell 16: 2910-2922.
44. Riha K, McKnight TD, Griffing LR, Shippen DE. 2001. Living with genome instability: Plant responses to telomere dysfunction. Science 291: 1797-1800.
45. Ruijter JM, Ramakers C, Hoogaars WM, Karlen Y, Bakker O, van den Hoff MJ, Moorman AF. 2009. Amplification efficiency: Linking baseline and bias in the analysis of quantitative PCR data. Nucleic Acids Res 37: e45. doi: 10.1093/nar/gkp045.
46. Samach A, Melamed-Bessudo C, Avivi-Ragolski N, Pietrokovski S, Levy AA. 2011. Identification of plant RAD52 homologs and characterization of the Arabidopsis thaliana RAD52-like genes. Plant Cell 23: 4266-4279.
47. Sarin KY, Cheung P, Gilison D, Lee E, Tennen RI, Wang E, Artandi MK, Oro AE, Artandi SE. 2005. Conditional telomerase induction causes proliferation of hair follicle stem cells. Nature 436: 1048-1052.
48. Shakirov EV, Surovtseva YV, Osbun N, Shippen DE. 2005. The Arabidopsis Pot1 and Pot2 proteins function in telomere length homeostasis and chromosome end protection. Mol Cell Biol 25: 7725-7733.
49. Shakirov EV, McKnight TD, Shippen DE. 2009. POT1-independent single-strand telomeric DNA binding activities in Brassicaceae. Plant J 58: 1004-1015.
50. Surovtseva YV, Shakirov EV, Vespa L, Osbun N, Song X, Shippen DE. 2007. Arabidopsis POT1 associates with the telomerase RNP and is required for telomere maintenance. EMBO J 26: 3653-3661.
51. Surovtseva YV, Churikov D, Boltz KA, Song X, Lamb JC, Warrington R, Leehy K, Heacock M, Price CM, Shippen DE. 2009. Conserved telomere maintenance component 1 interacts with STN1 and maintains chromosome ends in higher eukaryotes. Mol Cell 36: 207-218.
52. Tang W, Kannan R, Blanchette M, Baumann P. 2012. Telomerase RNA biogenesis involves sequential binding by Sm and Lsm complexes. Nature 484: 260-264.
53. Tesmer VM, Ford LP, Holt SE, Frank BC, Yi X, Aisner DL, Ouellette M, Shay JW, Wright WE. 1999. Two inactive fragments of the integral RNA cooperate to assemble active telomerase with the human protein catalytic subunit (hTERT) in vitro. Mol Cell Biol 19: 6207-6216.
54. Wang KC, Chang HY. 2011. Molecular mechanisms of long noncoding RNAs. Mol Cell 43: 904-914.
55. Wei W, Ba Z, Gao M, Wu Y, Ma Y, Amiard S, White CI, Rendtlew Danielsen JM, Yang YG, Qi Y. 2012. A role for small RNAs in DNA double-strand break repair. Cell 149: 101-112.
56. Wong JM, Kusdra L, Collins K. 2002. Subnuclear shuttling of human telomerase induced by transformation and DNA damage. Nat Cell Biol 4: 731-736.
57. Wouters MD, van Gent DC, Hoeijmakers JH, Pothof J. 2011. MicroRNAs, the DNA damage response and cancer. Mutat Res 717: 54-66.
58. Yu GL, Bradley JD, Attardi LD, Blackburn EH. 1990. In vivo alteration of telomere sequences and senescence caused by mutated Tetrahymena telomerase RNAs. Nature 344: 126-132.
59. Zappulla DC, Goodrich K, Cech TR. 2005. A miniature yeast telomerase RNA functions in vivo and reconstitutes activity in vitro. Nat Struct Mol Biol 12: 1072-1077.
60. Zhang W, Durocher D. 2010. De novo telomere formation is suppressed by the Mec1-dependent inhibition of Cdc13 accumulation at DNA breaks. Genes Dev 24: 502-515.
61. Zhu J, Wang H, Bishop JM, Blackburn EH. 1999. Telomerase extends the lifespan of virus-transformed human cells without net telomere lengthening. Proc Natl Acad Sci 96: 3723-3728