TRF2 inhibits a cell-extrinsic pathway through which natural killer cells eliminate cancer cells

Nature Cell Biology

Volumn 15, Issue 7, 2013, Pages 818-828

  Biroccio, Annamaria ^a,b   Cherfils Vicini, Julien ^c   Augereau, Adeline ^a,c   Pinte, Sébastien ^a,q   Bauwens, Serge ^a   Ye, Jing ^a,c,d   Simonet, Thomas ^a   Horard, Béatrice ^a   Jamet, Karine ^c   Cervera, Ludovic ^c   Mendez Bermudez, Aaron ^c   Poncet, Delphine ^a,q   Grataroli, Renée ^a   De Rodenbeeke, Claire T'Kint ^a   Salvati, Erica ^b   Rizzo, Angela ^b   Zizza, Pasquale ^b   Ricoul, Michelle ^e   Cognet, Céline ^f,g   Kuilman, Thomas ^h   Duret, Helene ⁱ   Lépinasse, Florian ^j,k   Marvel, Jacqueline ^l   Verhoeyen, Els ^a   Cosset, François Loïc ^a   Peeper, Daniel ^h   Smyth, Mark J ^i,m   Londoño Vallejo, Arturo ⁿ   Sabatier, Laure ^e   Picco, Vincent ^c   Pages, Gilles ^c   Scoazec, Jean Yves ^j,k   Stoppacciaro, Antonella ^o   Leonetti, Carlo ^b   Vivier, Eric ^f,g   Gilson, Eric ^a,c,l,p   more..

^a UNIVERSITÉ DE LYON   (France)

^b REGINA ELENA NATIONAL CANCER INSTITUTE   (Italy)

^c UNIVERSITY OF NICE SOPHIA ANTIPOLIS   (France)

^d SHANGHAI JIAO TONG UNIVERSITY   (China)

^e INSTITUT DE RADIOPROTECTION ET DE SÛRETÉ NUCLÉAIRE   (France)

^f AIX MARSEILLE UNIVERSITY   (France)

^g HÔPITAL DE LA CONCEPTION   (France)

^h NETHERLANDS CANCER INSTITUTE   (Netherlands)

ⁱ PETER MACCALLUM CANCER CENTRE   (Australia)

^j EDOUARD HERRIOT HOSPITAL   (France)

^k INSERM   (France)

^l UNIVERSITÉ LYON 1   (France)

^m QIMR BERGHOFER MEDICAL RESEARCH INSTITUTE   (Australia)

ⁿ INSTITUT CURIE   (France)

^o SAPIENZA UNIVERSITY OF ROME   (Italy)

^p CENTRE HOSPITALIER UNIVERSITAIRE DE NICE   (France)

^q INSTITUT PASTEUR DE LILLE   (France)

more..

Author keywords

[No Author keywords available]

Indexed keywords

HEPARAN SULPHATE (GLUCOSAMINE) 3 O SULFOTRANSFERASE 4; SULFOTRANSFERASE; TELOMERIC REPEAT BINDING FACTOR 2; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER CELL; CARCINOGENICITY; CELL DENSITY; CELLULAR IMMUNITY; COLON CANCER; COLON CARCINOGENESIS; CONTROLLED STUDY; EPISTASIS; GENE EXPRESSION REGULATION; HS3ST4 GENE; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOREGULATION; LYMPHOCYTE ACTIVATION; MALE; MOUSE; NATURAL KILLER CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; SIGNAL TRANSDUCTION;

ANIMALS; APOPTOSIS; BLOTTING, WESTERN; BREAST NEOPLASMS; CELL ADHESION; CELL PROLIFERATION; COLONIC NEOPLASMS; DNA PRIMERS; FEMALE; FLOW CYTOMETRY; HELA CELLS; HUMANS; KILLER CELLS, NATURAL; LYMPHOCYTES, TUMOR-INFILTRATING; MELANOMA, EXPERIMENTAL; MICE; MICE, NUDE; REAL-TIME POLYMERASE CHAIN REACTION; RECEPTOR PROTEIN-TYROSINE KINASES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; RNA, SMALL INTERFERING; SULFOTRANSFERASES; TELOMERIC REPEAT BINDING PROTEIN 2; TUMOR CELLS, CULTURED;

EID: 84880332846     PISSN: 14657392     EISSN: 14764679     Source Type: Journal    
DOI: 10.1038/ncb2774     Document Type: Article

References (61)

1. Blackburn, E. H., Greider, C. W. & Szostak, J. W. Telomeres and telomerase:the path from maize, Tetrahymena and yeast to human cancer and ageing. Nat. Med. 12, 1133-1138 (2006).
2. Blackburn, E. H. Telomere states and cell fates. Nature 408, 53-56 (2000).
3. d'Adda di Fagagna, F. et al. A DNA damage checkpoint response in telomere-initiated senescence. Nature 426, 194-198 (2003).
4. Rudolph, K. L., Millard, M., Bosenberg, M. W. & DePinho, R. A. Telomere dysfunction and evolution of intestinal carcinoma in mice and humans. Nat. Genet. 28, 155-159 (2001).
5. Gonzalez-Suarez, E., Samper, E., Flores, J. M. & Blasco, M. A. Telomerase-de-cient mice with short telomeres are resistant to skin tumorigenesis. Nat. Genet. 26, 114-117 (2000).
6. Guo, X. et al. Dysfunctional telomeres activate an ATM-ATR-dependent DNA damage response to suppress tumorigenesis. EMBO J. 26, 4709-4719 (2007).
7. Feldser, D. M. & Greider, C. W. Short telomeres limit tumour progression in vivo by inducing senescence. Cancer Cell 11, 461-469 (2007).
8. Cosme-Blanco, W. et al. Telomere dysfunction suppresses spontaneous tumorigenesis in vivo by initiating p53-dependent cellular senescence. EMBO Rep. 8, 497-503 (2007).
9. Ding, Z. et al. Telomerase reactivation following telomere dysfunction yields murine prostate tumours with bone metastases. Cell 148, 896-907 (2012).
10. Cech, T. R. Beginning to understand the end of the chromosome. Cell 116, 273-279 (2004).
11. Giraud-Panis, M. J. et al. One identity or more for telomeres? Front Oncol. 3, 48 (2013).
12. De Lange, T. Shelterin:the protein complex that shapes and safeguards human telomeres. Genes Dev. 19, 2100-2110 (2005).
13. Broccoli, D., Smogorzewska, A., Chong, L. & de Lange, T. Human telomeres contain two distinct Myb-related proteins, TRF1 and TRF2. Nat. Genet. 17, 231-235 (1997).
14. Bilaud, T. et al. Telomeric localization of TRF2, a novel human telobox protein. Nat. Genet. 17, 236-239 (1997).
15. Celli, G. B. & de Lange, T. DNA processing is not required for ATM-mediated telomere damage response after TRF2 deletion. Nat. Cell Biol. 7, 712-718 (2005).
16. Karlseder, J., Broccoli, D., Dai, Y., Hardy, S. & de Lange, T. p53- and ATM-dependent apoptosis induced by telomeres lacking TRF2. Science 283, 1321-1325 (1999).
17. Van Steensel, B., Smogorzewska, A. & de Lange, T. TRF2 protects human telomeres from end-to-end fusions. Cell 92, 401-413 (1998).
18. Okamoto, K. et al. A two-step mechanism for TRF2-mediated chromosome-end protection. Nature 494, 502-505 (2013).
19. Grif-th, J. D. et al. Mammalian telomeres end in a large duplex loop [see comments]. Cell 97, 503-514 (1999).
20. Amiard, S. et al. A topological mechanism for TRF2-enhanced strand invasion. Nat. Struct. Mol. Biol. 14, 147-154 (2007).
21. Nakanishi, K. et al. Expression of mRNAs for telomeric repeat binding factor (TRF)-1 and TRF2 in atypical adenomatous hyperplasia and adenocarcinoma of the lung. Clin. Cancer Res. 9, 1105-1111 (2003).
22. Begemann, S., Galimi, F. & Karlseder, J. Moderate expression of TRF2 in the hematopoietic system increases development of large cell blastic T-cell lymphomas. Aging 1, 122-130 (2009).
23. Bellon, M. et al. Increased expression of telomere length regulating factors TRF1, TRF2 and TIN2 in patients with adult T-cell leukaemia. Int. J. Cancer 119, 2090-2097 (2006).
24. Diehl, M. C. et al. Elevated TRF2 in advanced breast cancers with short telomeres. Breast Cancer Res. Treat. 127, 623-630 (2011).
25. Hu, H., Zhang, Y., Zou, M., Yang, S. & Liang, X. Q. Expression of TRF1, TRF2, TIN2, TERT, KU70, and BRCA1 proteins is associated with telomere shortening and may contribute to multistage carcinogenesis of gastric cancer. J. Cancer Res. Clin. Oncol. 136, 1407-1414 (2010).
26. Hsu, C. P., Ko, J. L., Shai, S. E. & Lee, L. W. Modulation of telomere shelterin by TRF1 [corrected] and TRF2 interacts with telomerase to maintain the telomere length in non-small cell lung cancer. Lung Cancer 58, 310-316 (2007).
27. Ning, H. et al. TRF2 promotes multidrug resistance in gastric cancer cells. Cancer Biol. Ther. 5, 950-956 (2006).
28. Oh, B. K., Kim, Y. J., Park, C. & Park, Y. N. Up-regulation of telomere-binding proteins, TRF1, TRF2, and TIN2 is related to telomere shortening during human multistep hepatocarcinogenesis. Am. J. Pathol. 166, 73-80 (2005).
29. Dong, W. et al. Sp1 upregulates expression of TRF2 and TRF2 inhibition reduces tumorigenesis in human colorectal carcinoma cells. Cancer Biol. Ther. 8, 2166-2174 (2009).
30. Dong, W., Wang, L., Chen, X., Sun, P. & Wu, Y. Upregulation and CpG island hypomethylation of the TRF2 gene in human gastric cancer. Dig. Dis. Sci. 55, 997-1003.
31. Biroccio, A. et al. TRF2 inhibition triggers apoptosis and reduces tumourigenicity of human melanoma cells. Eur. J. Cancer 42, 1881-1888 (2006).
32. Blanco, R., Munoz, P., Flores, J. M., Klatt, P. & Blasco, M. A. Telomerase abrogation dramatically accelerates TRF2-induced epithelial carcinogenesis. Genes Dev. 21, 206-220 (2007).
33. Diala, I. et al. Telomere protection and TRF2 expression are enhanced by the canonical Wnt signalling pathway. EMBO Rep. 14, 356-363 (2013).
34. Teo, H. et al. Telomere-independent Rap1 is an IKK adaptor and regulates NF-B-dependent gene expression. Nat. Cell Biol. 12, 758-767 (2010).
35. Takai, K. K., Hooper, S., Blackwood, S., Gandhi, R. & de Lange, T. In vivo stoichiometry of shelterin components. J. Biol. Chem. 285, 1457-1467 (2010).
36. Ancrile, B., Lim, K. H. & Counter, C. M. Oncogenic Ras-induced secretion of IL6 is required for tumorigenesis. Genes Dev. 21, 1714-1719 (2007).
37. Coppe, J. P. et al. Senescence-associated secretory phenotypes reveal cellnonautonomous functions of oncogenic RAS and the p53 tumour suppressor. PLoS Biol. 6, 2853-2868 (2008).
38. Kuilman, T. et al. Oncogene-induced senescence relayed by an interleukindependent in-ammatory network. Cell 133, 1019-1031 (2008).
39. Kozma, S. C. et al. The human c-Kirsten ras gene is activated by a novel mutation in codon 13 in the breast carcinoma cell line MDA-MB231. Nucleic Acids Res. 15, 5963-5971 (1987).
40. Naldini, A. & Carraro, F. Role of in-ammatory mediators in angiogenesis. Curr. Drug Targets In-amm. Allergy 4, 3-8 (2005).
41. Lau, A. et al. Suppression of HIV-1 infection by a small molecule inhibitor of the ATM kinase. Nat. Cell Biol. 7, 493-500 (2005).
42. Denchi, E. L. & de Lange, T. Protection of telomeres through independent control of ATM and ATR by TRF2 and POT1. Nature 448, 1068-1071 (2007).
43. Gasser, S., Orsulic, S., Brown, E. J. & Raulet, D. H. The DNA damage pathway regulates innate immune system ligands of the NKG2D receptor. Nature 436, 1186-1190 (2005).
44. Soriani, A. et al. ATM-ATR-dependent up-regulation of DNAM-1 and NKG2D ligands on multiple myeloma cells by therapeutic agents results in enhanced NK-cell susceptibility and is associated with a senescent phenotype. Blood 113, 3503-3511 (2009).
45. Brandt, C. S. et al. The B7 family member B7-H6 is a tumour cell ligand for the activating natural killer cell receptor NKp30 in humans. J. Exp. Med. 206, 1495-1503 (2009).
46. Kuilman, T. & Peeper, D. S. Senescence-messaging secretome:SMS-ing cellular stress. Nat. Rev. Cancer 9, 81-94 (2009).
47. Simonet, T. et al. The human TTAGGG repeat factors 1 and 2 bind to a subset of interstitial telomeric sequences and satellite repeats. Cell Res. 21, 1028-1038 (2011).
48. Ruiz-Herrera, A., Nergadze, S. G., Santagostino, M. & Giulotto, E. Telomeric repeats far from the ends:mechanisms of origin and role in evolution. Cytogenet. Genome Res. 122, 219-228 (2008).
49. Bishop, J. R., Schuksz, M. & Esko, J. D. Heparan sulphate proteoglycans -ne-tune mammalian physiology. Nature 446, 1030-1037 (2007).
50. Hacker, U., Nybakken, K. & Perrimon, N. Heparan sulphate proteoglycans:the sweet side of development. Nat. Rev. Mol. Cell Biol. 6, 530-541 (2005).
51. Feizi, T. Carbohydrate-mediated recognition systems in innate immunity. Immunol. Rev. 173, 79-88 (2000).
52. Zhang, Y. W., Zhang, Z. X., Miao, Z. H. & Ding, J. The telomeric protein TRF2 is critical for the protection of A549 cells from both telomere erosion and DNA doublestrand breaks driven by salvicine. Mol. Pharmacol. 73, 824-832 (2008).
53. Yang, D. et al. Human telomeric proteins occupy selective interstitial sites. Cell Res. 21, 1013-1027 (2011).
54. Marcand, S., Buck, S. W., Moretti, P., Gilson, E. & Shore, D. Silencing of genes at nontelomeric sites in yeast is controlled by sequestration of silencing factors at telomeres by Rap1 protein. Genes Dev. 10, 1297-1309 (1996).
55. Maillet, L. et al. Evidence for silencing compartments within the yeast nucleus :A role for telomere proximity and Sir-protein concentration in silencer-mediated repression. Genes Dev. 10, 1796-1811 (1996).
56. Hahn, W. C. et al. Creation of human tumour cells with de-ned genetic elements. Nature 400, 464-468 (1999).
57. Counter, C. M. et al. Telomere shortening associated with chromosome instability is arrested in immortal cells which express telomerase activity. EMBO J. 11, 1921-1929 (1992).
58. Salmon, P. & Trono, D. Production and titration of lentiviral vectors. Curr. Protoc. Hum. Genet. http://dx.doi.org/10.1002/0471142905. hg1210s54 (2007).
59. Leonetti, C. et al. Antitumour effect of c-myc antisense phosphorothioate oligodeoxynucleotides on human melanoma cells in vitro and and in mice. J. Natl. Cancer Inst. 88, 419-429 (1996).
60. Spanopoulou, E. et al. Functional immunoglobulin transgenes guide ordered B-cell differentiation in Rag-1-de-cient mice. Genes Dev. 8, 1030-1042 (1994).
61. Schlemper, R. J. et al. The Vienna classi-cation of gastrointestinal epithelial neoplasia. Gut 47, 251-255 (2000).