Formation of telomeric repeat-containing RNA (TERRA) foci in highly proliferating mouse cerebellar neuronal progenitors and medulloblastoma

Journal of Cell Science

Volumn 125, Issue 18, 2012, Pages 4383-4394

  Deng, Zhong ^a   Wang, Zhuo ^a   Xiang, Chaomei ^a,b   Molczan, Aliah ^a   Baubet, Valé rie ^a,b   Conejo Garcia, Jose ^a   Xu, Xiaowei ^b   Lieberman, Paul M ^a   Dahmane, Nadia ^a,b  

^a WISTAR INSTITUTE   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Cancer; Cerebellum; Medulloblastoma; Neuronal progenitors; Sonic hedgehog; Telomere repeat containing non coding RNA; Terra

Indexed keywords

HISTONE H2AX; SONIC HEDGEHOG PROTEIN; TELOMERE BINDING PROTEIN; TELOMERIC REPEAT CONTAINING RNA; UNCLASSIFIED DRUG; UNTRANSLATED RNA;

ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL PROLIFERATION; COILED BODY; CONTROLLED STUDY; DNA DAMAGE; DNA DAMAGE CHECKPOINT; HUMAN; HUMAN TISSUE; IN VITRO STUDY; MEDULLOBLASTOMA; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMYELOCYTIC LEUKEMIA; PROTEIN EXPRESSION; TUMOR BIOPSY;

ANIMALS; BRAIN; CELL PROLIFERATION; CEREBELLAR NEOPLASMS; COILED BODIES; DISEASE MODELS, ANIMAL; DNA DAMAGE; GENE EXPRESSION REGULATION, NEOPLASTIC; HEDGEHOG PROTEINS; HISTONES; HUMANS; IN SITU HYBRIDIZATION, FLUORESCENCE; INTERPHASE; MEDULLOBLASTOMA; MICE; MODELS, BIOLOGICAL; NEURAL STEM CELLS; REPETITIVE SEQUENCES, NUCLEIC ACID; RNA; TELOMERE;

ERINACEIDAE; EUKARYOTA; MAMMALIA;

EID: 84868513499     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.108118     Document Type: Article

References (68)

1. Armentano, M., Filosa, A., Andolfi, G. and Studer, M. (2006). Coup-TFI is required for the formation of commisural projections in the forebrain by regulating axonal growth. Development 133, 4151-4162.
2. Azzalin, C. M., Reichenbach, P., Khoriauli, L., Giulotto, E. and Lingner, J. (2007). Telomeric repeat containing RNA and RNA surveillance factors at mammalian chromosome ends. Science 318, 798-801.
3. Baerlocher, G. M., Vulto, I., de Jong, G. and Lansdorp, P. M. (2006). Flow cytometry and FISH to measure the average length of telomeres (flow FISH). Nat. Protoc. 1, 2365-2376.
4. Bah, A., Wischnewski, H., Shchepachev, V. and Azzalin, C. M. (2012). The telomeric transcriptome of Schizosaccharomyces pombe. Nucleic Acids Res. 40, 2995-3005.
5. Bartkova, J., Horejsi{dotless}́, Z., Koed, K., Krämer, A., Tort, F., Zieger, K., Guldberg, P., Sehested, M., Nesland, J. M., Lukas, C. et al. (2005). DNA damage response as a candidate anti-cancer barrier in early human tumorigenesis. Nature 434, 864-870.
6. Biamonti, G. and Vourc'h, C. (2010). Nuclear stress bodies. Cold Spring Harb. Perspect. Biol. 2, a000695.
7. Blackburn, E. H., Grieder, C. W. and Szostak, J. W. (2006). Telomeres and Telomerase: the path from maize, Tetrahymena, and yeast to human cancer and aging. Nat. Med. 12, 1133-1338.
8. Blasco, M. A. (2005). Telomeres and human disease: ageing, cancer and beyond. Nat. Rev. Genet. 6, 611-622.
9. Blasco, M. A. (2007). Telomere length, stem cells and aging. Nat. Chem. Biol. 3, 640-649.
10. Caslini, C., Connelly, J. A., Serna, A., Broccoli, D. and Hess, J. L. (2009). MLL associates with telomeres and regulates telomeric repeat-containing RNA transcription. Mol. Cell. Biol. 29, 4519-4526.
11. Cech, T. R. (2004). Beginning to understand the end of the chromosome. Cell. 116, 273-279.
12. Corcoran, R. B. and Scott, M. P. (2001). A mouse model for medulloblastoma and basal cell nevus syndrome. J. Neurooncol. 53, 307-318.
13. d'Adda di Fagagna, F., Reaper, P. M., Clay-Farrace, L., Fiegler, H., Carr, P., Von Zglinicki, T., Saretzki, G., Carter, N. P. and Jackson, S. P. (2003). A DNA damage checkpoint response in telomere-initiated senescence. Nature 426, 194-198.
14. Dahmane, N. and Ruiz i Altaba, A. (1999). Sonic hedgehog regulates the growth and patterning of the cerebellum. Development 126, 3089-3100.
15. de Lange, T. (2002). Protection of mammalian telomeres. Oncogene 21, 532-540.
16. de Lange, T. (2004). T-loops and the origin of telomeres. Nat. Rev. Mol. Cell Biol. 5, 323-329.
17. de Lange, T. (2005a). Shelterin: the protein complex that shapes and safeguards human telomeres. Genes Dev. 19, 2100-2110.
18. De Lange, T. (2005b). Telomere-related genome instability in cancer. Cold Spring Harb. Symp. Quant. Biol. 70, 197-204.
19. Deng, Z., Norseen, J., Wiedmer, A., Riethman, H. and Lieberman, P. M. (2009). TERRA RNA binding to TRF2 facilitates heterochromatin formation and ORC recruitment at telomeres. Mol. Cell 35, 403-413.
20. Ellison, D. (2002). Classifying the medulloblastoma: insights from morphology and molecular genetics. Neuropathol. Appl. Neurobiol. 28, 257-282.
21. Ellison, D. W. (2010). Childhood medulloblastoma: novel approaches to the classification of a heterogeneous disease. Acta Neuropathol. 120, 305-316.
22. El-Zaatari, M., Tobias, A., Grabowska, A. M., Kumari, R., Scotting, P. J., Kaye, P., Atherton, J., Clarke, P. A., Powe, D. G. and Watson, S. A. (2007). De-regulation of the sonic hedgehog pathway in the InsGas mouse model of gastric carcinogenesis. Br. J. Cancer. 96, 1855-1861.
23. Ferlicot, S., Durrbach, A., Ba, N., Desvaux, D., Bedossa, P. and Paradis, V. (2003). The role of replicative senescence in chronic allograft nephropathy. Hum. Pathol. 34, 924-928.
24. Fernandez, C., Tatard, V. M., Bertrand, N. and Dahmane, N. (2010). Differential modulation of Sonic-hedgehog-induced cerebellar granule cell precursor proliferation by the IGF signaling network. Dev. Neurosci. 32, 59-70.
25. Flynn, R. L., Centore, R. C., O'Sullivan, R. J., Rai, R., Tse, A., Songyang, Z., Chang, S., Karlseder, J. and Zou, L. (2011). TERRA and hnRNPA1 orchestrate an RPA-to-POT1 switch on telomeric single-stranded DNA. Nature 471, 532-536.
26. Fragkos, M., Jurvansuu, J. and Beard, P. (2009). H2AX is required for cell cycle arrest via the p53/p21 pathway. Mol. Cell. Biol. 29, 2828-2840.
27. Gilbertson, R. J. (2004). Medulloblastoma: signalling a change in treatment. Lancet Oncol. 5, 209-218.
28. Gilbertson, R. J. and Ellison, D. W. (2008). The origins of medulloblastoma subtypes. Annu. Rev. Pathol. 3, 341-365.
29. Goodrich, L. V., Milenković, L., Higgins, K. M. and Scott, M. P. (1997). Altered neural cell fates and medulloblastoma in mouse patched mutants. Science 277, 1109-1113.
30. Gorgoulis, V. G., Vassiliou, L. V., Karakaidos, P., Zacharatos, P., Kotsinas, A., Liloglou, T., Venere, M., Ditullio, R. A., Jr, Kastrinakis, N. G., Levy, B. et al. (2005). Activation of the DNA damage checkpoint and genomic instability in human precancerous lesions. Nature 434, 907-913.
31. Greenwood, J. and Cooper, J. P. (2012). Non-coding telomeric and subtelomeric transcripts are differentially regulated by telomeric and heterochromatin assembly factors in fission yeast. Nucleic Acids Res.40, 2956-2963.
32. Hahn, H., Wicking, C., Zaphiropoulous, P. G., Gailani, M. R., Shanley, S., Chidambaram, A., Vorechovsky, I., Holmberg, E., Unden, A. B., Gillies, S. et al. (1996). Mutations of the human homolog of Drosophila patched in the nevoid basal cell carcinoma syndrome. Cell 85, 841-851.
33. Jackson, S. P. and Bartek, J. (2009). The DNA-damage response in human biology and disease. Nature 461, 1071-1078.
34. Jain, D. and Cooper, J. P. (2010). Telomeric strategies: means to an end. Annu. Rev. Genet. 44, 243-269.
35. Johnson, R. L., Rothman, A. L., Xie, J., Goodrich, L. V., Bare, J. W., Bonifas, J. M., Quinn, A. G., Myers, R. M., Cox, D. R., Epstein, E. H., Jr et al. (1996). Human homolog of patched, a candidate gene for the basal cell nevus syndrome. Science 272, 1668-1671.
36. Kho, A. T., Zhao, Q., Cai, Z., Butte, A. J., Kim, J. Y., Pomeroy, S. L., Rowitch, D. H. and Kohane, I. S. (2004). Conserved mechanisms across development and tumorigenesis revealed by a mouse development perspective of human cancers. Genes Dev. 18, 629-640.
37. Liu, D., O'Connor, M. S., Qin, J. and Songyang, Z. (2004). Telosome, a mammalian telomere-associated complex formed by multiple telomeric proteins. J. Biol. Chem. 279, 51338-51342.
38. López de Silanes, I., Stagno d'Alcontres, M. and Blasco, M. A. (2010). TERRA transcripts are bound by a complex array of RNA-binding proteins. Nat. Commun. 1, 33.
39. Mai, S. and Garini, Y. (2006). The significance of telomeric aggregates in the interphase nuclei of tumor cells. J. Cell. Biochem. 97, 904-915.
40. Marion, R. M., Strati, K., Li, H., Tejera, A., Schoeftner, S., Ortega, S., Serrano, M. and Blasco, M. A. (2009). Telomeres acquire embryonic stem cell characteristics in induced pluripotent stem cells. Cell Stem Cell 4, 141-154.
41. Ng, L. J., Cropley, J. E., Pickett, H. A., Reddel, R. R. and Suter, C. M. (2009). Telomerase activity is associated with an increase in DNA methylation at the proximal subtelomere and a reduction in telomeric transcription. Nucleic Acids Res. 37, 1152-1159.
42. Oliver, T. G., Read, T. A., Kessler, J. D., Mehmeti, A., Wells, J. F., Huynh, T. T., Lin, S. M. and Wechsler-Reya, R. J. (2005). Loss of patched and disruption of granule cell development in a pre-neoplastic stage of medulloblastoma. Development 132, 2425-2439.
43. Palm, W. and de Lange, T. (2008). How shelterin protects mammalian telomeres. Annu. Rev. Genet. 42, 301-334.
44. Parker, R. and Sheth, U. (2007). P bodies and the control of mRNA translation and degradation. Mol. Cell 25, 635-646.
45. Raynaud, C. M., Hernandez, J., Llorca, F. P., Nuciforo, P., Mathieu, M. C., Commo, F., Delaloge, S., Sabatier, L., André, F. and Soria, J. C. (2010). DNA damage repair and telomere length in normal breast, preneoplastic lesions, and invasive cancer. Am. J. Clin. Oncol. 33, 341-345.
46. Raz, V., Vermolen, B. J., Garini, Y., Onderwater, J. J., Mommaas-Kienhuis, M. A., Koster, A. J., Young, I. T., Tanke, H. and Dirks, R. W. (2008). The nuclear lamina promotes telomere aggregation and centromere peripheral localization during senescence of human mesenchymal stem cells. J. Cell Sci. 121, 4018-4028.
47. Redon, S., Reichenbach, P. and Lingner, J. (2010). The non-coding RNA TERRA is a natural ligand and direct inhibitor of human telomerase. Nucleic Acids Res. 38, 5797-5806.
48. Ruiz i Altaba, A., Sánchez, P. and Dahmane, N. (2002). Gli and hedgehog in cancer: tumours, embryos and stem cells. Nat. Rev. Cancer 2, 361-372.
49. Sahin, E. and Depinho, R. A. (2010). Linking functional decline of telomeres, mitochondria and stem cells during ageing. Nature 464, 520-528.
50. Sampl, S., Pramhas, S., Stern, C., Preusser, M., Marosi, C. and Holzmann, K. (2012). Expression of telomeres in astrocytoma WHO Grade 2 to 4: TERRA level correlates with telomere lenght, telomerase activity, and advanced clinical grade. Transl. Oncol. 5, 56-65.
51. Schoeftner, S. and Blasco, M. A. (2008). Developmentally regulated transcription of mammalian telomeres by DNA-dependent RNA polymerase II. Nat. Cell Biol. 10, 228-236.
52. Schoeftner, S., Blanco, R., Lopez de Silanes, I., Mun{ogonek} oz, P., Gómez-López, G., Flores, J. M. and Blasco, M. A. (2009). Telomere shortening relaxes X chromosome inactivation and forces global transcriptome alterations. Proc. Natl. Acad. Sci. USA 106, 19393-19398.
53. Sedelnikova, O. A. and Bonner, W. M. (2006). GammaH2AX in cancer cells: a potential biomarker for cancer diagnostics, prediction and recurrence. Cell Cycle 5, 2909-2913.
54. Shevtsov, S. P. and Dundr, M. (2011). Nucleation of nuclear bodies by RNA. Nat. Cell Biol. 13, 167-173.
55. Takai, H., Smogorzewska, A. and de Lange, T. (2003). DNA damage foci at dysfunctional telomeres. Curr. Biol. 13, 1549-1556.
56. Ting, D. T., Lipson, D., Paul, S., Brannigan, B. W., Akhavanfard, S., Coffman, E. J., Contino, G., Deshpande, V., Iafrate, A. J., Letovsky, S. et al. (2011). Aberrant overexpression of satellite repeats in pancreatic and other epithelial cancers. Science 331, 593-596.
57. Toledo, L. I., Murga, M., Zur, R., Soria, R., Rodriguez, A., Martinez, S., Oyarzabal, J., Pastor, J., Bischoff, J. R. and Fernandez-Capetillo, O. (2011). A cell-based screen identifies ATR inhibitors with synthetic lethal properties for cancer-associated mutations. Nat. Struct. Mol. Biol. 18, 721-727.
58. Wallace, V. A. (1999). Purkinje-cell-derived Sonic hedgehog regulates granule neuron precursor cell proliferation in the developing mouse cerebellum. Curr. Biol. 9, 445-448.
59. Wechsler-Reya, R. J. and Scott, M. P. (1999). Control of neuronal precursor proliferation in the cerebellum by Sonic Hedgehog. Neuron 22, 103-114.
60. Wentzensen, I. M., Mirabello, L., Pfeiffer, R. M. and Savage, S. A. (2011). The association of telomere length and cancer: a meta-analysis. Cancer Epidemiol. Biomarkers Prev. 20, 1238-1250.
61. Wileman, T. (2007). Aggresomes and pericentriolar sites of virus assembly: cellular defense or viral design? Annu. Rev. Microbiol. 61, 149-167.
62. Xiang, C., Baubet, V., Pal, S., Holderbaum, L., Tatard, V., Jiang, P., Davuluri, R. V. and Dahmane, N. (2012). RP58/ZNF238 directly modulates proneurogenic gene levels and is required for neuronal differentiation and brain expansion. Cell Death Differ. 19, 692-702.
63. Xu, L. and Blackburn, E. H. (2007). Human cancer cells harbor T-stumps, a distinct class of extremely short telomeres. Mol. Cell 28, 315-327.
64. Ye, J., Wu, Y. and Gilson, E. (2010). Dynamics of telomeric chromatin at the crossroads of aging and cancer. Essays Biochem. 48, 147-164.
65. Yehezkel, S., Segev, Y., Viegas-Péquignot, E., Skorecki, K. and Selig, S. (2008). Hypomethylation of subtelomeric regions in ICF syndrome is associated with abnormally short telomeres and enhanced transcription from telomeric regions. Hum. Mol. Genet. 17, 2776-2789.
66. Yehezkel, S., Rebibo-Sabbah, A., Segev, Y., Tzukerman, M., Shaked, R., Huber, I., Gepstein, L., Skorecki, K. and Selig, S. (2011). Reprogramming of telomeric regions during the generation of human induced pluripotent stem cells and subsequent differentiation into fibroblast-like derivatives. Epigenetics 6, 63-75.
67. Zhang, L. F., Ogawa, Y., Ahn, J. Y., Namekawa, S. H., Silva, S. S. and Lee, J. T. (2009). Telomeric RNAs mark sex chromosomes in stem cells. Genetics 182, 685-698.
68. Zheng, J. L. and Gao, W. Q. (2000). Overexpresion of Math1 induces robust production of extra hair cells in postnatal rat inner ears. Nat. Neurosci. 3, 580-586.