Telomere targeting with a new G4 ligand enhances radiation-induced killing of human glioblastoma cells

Molecular Cancer Therapeutics

Volumn 10, Issue 10, 2011, Pages 1784-1795

  Merle, Patrick ^a,b   Evrard, Bertrand ^a,b   Petitjean, Anne ^d,e   Lehn, Jean Marie ^d   Teulade Fichou, Marie Paule ^f   Chautard, Emmanuel ^a,c   De Cian, Anne ^g   Guittat, Lionel ^g   Tran, Phong Lan Thao ^h   Mergny, Jean Louis ^g,h   Verrelle, Pierre ^a,c   Tchirkov, Andreï ^a,b,c  

^a UNIVERSITÉ CLERMONT AUVERGNE   (France)

^b UNIVERSITY HOSPITAL OF CLERMONT FERRAND   (France)

^c CENTRE JEAN PERRIN   (France)

^d UNIVERSITÉ DE STRASBOURG   (France)

^e QUEEN S UNIVERSITY   (Canada)

^f INSTITUT CURIE   (France)

^g MUSÉUM NATIONAL D'HISTOIRE NATURELLE   (France)

^h UNIVERSITÉ DE BORDEAUX   (France)

Author keywords

[No Author keywords available]

Indexed keywords

GUANINE QUADRUPLEX; HISTONE H2AX; RADIOSENSITIZING AGENT; TELOMERASE REVERSE TRANSCRIPTASE; TELOMERIC REPEAT BINDING FACTOR 1; TELOMERIC REPEAT BINDING FACTOR 2;

APOPTOSIS; ARTICLE; CELL PROLIFERATION; CELLULAR DISTRIBUTION; CLONOGENIC ASSAY; CONTROLLED STUDY; CYTOGENETICS; DICENTRIC CHROMOSOME; DNA DAMAGE; DNA REPAIR; GENE EXPRESSION; GENE TARGETING; GLIOBLASTOMA; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE TEST; IN VITRO STUDY; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RADIATION INDUCED NEOPLASM; SURVIVAL RATE; TELOMERE; TUMOR CELL LINE;

ADULT; BRAIN NEOPLASMS; CELL GROWTH PROCESSES; CELL LINE, TUMOR; COMBINED MODALITY THERAPY; DNA DAMAGE; FEMALE; G-QUADRUPLEXES; GLIOBLASTOMA; HUMANS; LIGANDS; MESYLATES; PYRIMIDINES; RADIATION-SENSITIZING AGENTS; TELOMERASE; TELOMERE;

EID: 80053973244     PISSN: 15357163     EISSN: 15388514     Source Type: Journal    
DOI: 10.1158/1535-7163.MCT-10-0664     Document Type: Article

References (50)

1. Stupp R, Mason WP, van den Bent MJ, Weller M, Fisher B, Taphoorn MJ, et al. Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med 2005;352:987-96. (Pubitemid 40349501)
2. Morin GB. The human telomere terminal transferase enzyme is a ribonucleoprotein that synthesizes TTAGGG repeats. Cell 1989;59:521-9. (Pubitemid 19284465)
3. Kim NW, Piatyszek MA, Prowse KR, Harley CB, West MD, Ho PL, et al. Specific association of human telomerase activity with immortal cells and cancer. Science 1994;266:2011-5.
4. Langford LA, Piatyszek MA, Xu R, Schold SC Jr, Shay JW. Telomerase activity in human brain tumours. Lancet 1995;346:1267-8.
5. Tchirkov A, Rolhion C, Kemeny JL, Irthum B, Puget S, Khalil T, et al. Clinical implications of quantitative real-time RT-PCR analysis of hTERT gene expression in human gliomas. Br J Cancer 2003;88:516-20. (Pubitemid 36363360)
6. Lin PC, Lin SZ, Chen YL, Chang JS, Ho LI, Liu PY, et al. Butylidenephthalide suppresses human telomerase reverse transcriptase (TERT) in human glioblastomas. Ann Surg Oncol 2011 May 7. [Epub ahead of print].
7. Marian CO, Cho SK, McEllin BM, Maher EA, Hatanpaa KJ, Madden CJ, et al. The telomerase antagonist, imetelstat, efficiently targets glioblastoma tumor-initiating cells leading to decreased proliferation and tumor growth. Clin Cancer Res 2010;16:154-63.
8. Wong KK, Chang S, Weiler SR, Ganesan S, Chaudhuri J, Zhu C, et al. Telomere dysfunction impairs DNA repair and enhances sensitivity to ionizing radiation. Nat Genet 2000;26:85-8.
9. Alberti P, Lacroix L, Guittat L, Helene C, Mergny JL. Nucleic acids as targets for antitelomerase agents. Mini Rev Med Chem 2003;3:23-36.
10. Neidle S, Parkinson GN. The structure of telomeric DNA. Curr Opin Struct Biol 2003;13:275-83. (Pubitemid 36782453)
11. Granotier C, Pennarun G, Riou L, Hoffschir F, Gauthier LR, De Cian A, et al. Preferential binding of a G-quadruplex ligand to human chromosome ends. Nucleic Acids Res 2005;33:4182-90. (Pubitemid 41487277)
12. Kelland L. Targeting the limitless replicative potential of cancer: the telomerase/telomere pathway. Clin Cancer Res 2007;13:4960-3. (Pubitemid 47502059)
13. Pennarun G, Granotier C, Gauthier LR, Gomez D, Hoffschir F, Mandine E, et al. Apoptosis related to telomere instability and cell cycle alterations in human glioma cells treated by new highly selective G-quadruplex ligands. Oncogene 2005;24:2917-28. (Pubitemid 40675523)
14. Rosu F, De Pauw E, Guittat L, Alberti P, Lacroix L, Mailliet P, et al. Selective interaction of ethidium derivatives with quadruplexes: an equilibrium dialysis and electrospray ionization mass spectrometry analysis. Biochemistry 2003;42:10361-71. (Pubitemid 37071436)
15. De Cian A, Guittat L, Kaiser M, Sacca B, Amrane S, Bourdoncle A, et al. Fluorescence-based melting assays for studying quadruplex ligands. Methods 2007;42:183-95. (Pubitemid 46667236)
16. Ohyashiki JH, Hisatomi H, Nagao K, Honda S, Takaku T, Zhang Y, et al. Quantitative relationship between functionally active telomerase and major telomerase components (hTERT and hTR) in acute leukaemia cells. Br J Cancer 2005;92:1942-7. (Pubitemid 40826145)
17. Lin X, Gu J, Lu C, Spitz MR, Wu X. Expression of telomere-associated genes as prognostic markers for overall survival in patients with nonsmall cell lung cancer. Clin Cancer Res 2006;12:5720-5. (Pubitemid 44629601)
18. Tchirkov A, Chaleteix C, Magnac C, Vasconcelos Y, Davi F, Michel A, et al. hTERT expression and prognosis in B-chronic lymphocytic leukemia. Ann Oncol 2004;15:1476-80. (Pubitemid 39409736)
19. Kwiatkowski F, Girard M, Hacene K, Berlie J. Sem: a suitable statistical software adaptated for research in oncology. Bull Cancer 2000;87:715-21.
20. Petitjean A, Khoury RG, Kyritsakas N, Lehn JM. Dynamic devices. Shape switching and substrate binding in ion-controlled nanomechanical molecular tweezers. J Am Chem Soc 2004;126:6637-47. (Pubitemid 38697362)
21. Crothers DM. Calculation of binding isotherms for heterogenous polymers. Biopolymers 1968;6:575-84.
22. McGhee JD, von Hippel PH. Theoretical aspects of DNA-protein interactions: co-operative and non-co-operative binding of large ligands to a one-dimensional homogeneous lattice. J Mol Biol 1974;86:469-89.
23. Bacolla A, Wells RD. Non-B DNA conformations as determinants of mutagenesis and human disease. Mol Carcinog 2009;48:273-85.
24. Monchaud D, Teulade-Fichou MP. A hitchhiker's guide to G-quadruplex ligands. Org Biomol Chem 2008;6:627-36. (Pubitemid 351972601)
25. Huppert JL. Four-stranded nucleic acids: structure, function and targeting of G-quadruplexes. Chem Soc Rev 2008;37:1375-84.
26. Neidle S. The structures of quadruplex nucleic acids and their drug complexes. Curr Opin Struct Biol 2009;19:239-50.
27. Carrasco C, Rosu F, Gabelica V, Houssier C, De Pauw E, Garbay- Jaureguiberry C, et al. Tight binding of the antitumor drug ditercalinium to quadruplex DNA. Chembiochem 2002;3:1235-41. (Pubitemid 36005316)
28. Granzhan A, Monchaud D, Saettel N, Guedin A, Mergny JL, Teulade- Fichou MP. "One Ring to Bind Them All"-part II: identification of promising G-quadruplex ligands by screening of cyclophane-type macrocycles. J Nucleic Acids 2010;2010:460561.
29. Kaiser M, De Cian A, Sainlos M, Renner C, Mergny JL, Teulade-Fichou MP. Neomycin-capped aromatic platforms: quadruplex DNA recognition and telomerase inhibition. Org Biomol Chem 2006;4:1049-57. (Pubitemid 43383351)
30. Teulade-Fichou MP, Carrasco C, Guittat L, Bailly C, Alberti P, Mergny JL, et al. Selective recognition of G-qQuadruplex telomeric DNA by a bis(quinacridine) macrocycle. J Am Chem Soc 2003;125:4732-40. (Pubitemid 36505365)
31. Xu L, Zhang D, Huang J, Deng M, Zhang M, Zhou X. High fluorescence selectivity and visual detection of G-quadruplex structures by a novel dinuclear ruthenium complex. Chem Commun (Camb) 2010;46:743-5.
32. Gabelica V, Baker ES, Teulade-Fichou MP, De Pauw E, Bowers MT. Stabilization and structure of telomeric and c-myc region intramolecular G-quadruplexes: the role of central cations and small planar ligands. J Am Chem Soc 2007;129:895-904. (Pubitemid 46183939)
33. De Cian A, Cristofari G, Reichenbach P, De Lemos E, Monchaud D, Teulade-Fichou MP, et al. Reevaluation of telomerase inhibition by quadruplex ligands and their mechanisms of action. Proc Natl Acad Sci U S A 2007;104:17347-52. (Pubitemid 350219845)
34. Salvati E, Leonetti C, Rizzo A, Scarsella M, Mottolese M, Galati R, et al. Telomere damage induced by the G-quadruplex ligand RHPS4 has an antitumor effect. J Clin Invest 2007;117:3236-47. (Pubitemid 350096981)
35. Chautard E, Loubeau G, Tchirkov A, Chassagne J, Vermot-Desroches C, Morel L, et al. Akt signaling pathway: a target for radiosensitizing human malignant glioma. Neuro Oncol 2010;12:434-43.
36. MacPhail SH, Banath JP, Yu TY, Chu EH, Lambur H, Olive PL. Expression of phosphorylated histone H2AX in cultured cell lines following exposure to X-rays. Int J Radiat Biol 2003;79:351-8. (Pubitemid 36920536)
37. Leonetti C, Amodei S, D'Angelo C, Rizzo A, Benassi B, Antonelli A, et al. Biological activity of the G-quadruplex ligand RHPS4 (3,11-difluoro-6,8,13- trimethyl-8H-quino[4,3,2-kl]acridinium methosulfate) is associated with telomere capping alteration. Mol Pharmacol 2004;66:1138-46. (Pubitemid 39411054)
38. Incles CM, Schultes CM, Kempski H, Koehler H, Kelland LR, Neidle S. A G-quadruplex telomere targeting agent produces p16-associated senescence and chromosomal fusions in human prostate cancer cells. Mol Cancer Ther 2004;3:1201-6. (Pubitemid 39440164)
39. Gomez D, Paterski R, Lemarteleur T, Shin-Ya K, Mergny JL, Riou JF. Interaction of telomestatin with the telomeric single-strand overhang. J Biol Chem 2004;279:41487-94. (Pubitemid 39313589)
40. De Cian A, Lacroix L, Douarre C, Temime-Smaali N, Trentesaux C, Riou JF, et al. Targeting telomeres and telomerase. Biochimie 2008;90:131-55. (Pubitemid 350245369)
41. Gomez D, O'Donohue MF, Wenner T, Douarre C, Macadre J, Koebel P, et al. The G-quadruplex ligand telomestatin inhibits POT1 binding to telomeric sequences in vitro and induces GFP-POT1 dissociation from telomeres in human cells. Cancer Res 2006;66:6908-12. (Pubitemid 44197664)
42. Gomez D, Aouali N, Renaud A, Douarre C, Shin-Ya K, Tazi J, et al. Resistance to senescence induction and telomere shortening by a G-quadruplex ligand inhibitor of telomerase. Cancer Res 2003;63:6149-53. (Pubitemid 37255154)
43. Smogorzewska A, van Steensel B, Bianchi A, Oelmann S, Schaefer MR, Schnapp G, et al. Control of human telomere length by TRF1 and TRF2. Mol Cell Biol 2000;20:1659-68. (Pubitemid 30100185)
44. Wedge SR, Porteous JK, Glaser MG, Marcus K, Newlands ES. In vitro evaluation of temozolomide combined with X-irradiation. Anticancer Drugs 1997;8:92-7. (Pubitemid 27064756)
45. van Rijn J, Heimans JJ, van den Berg J, van der Valk P, Slotman BJ. Survival of human glioma cells treated with various combination of temozolomide and X-rays. Int J RadiatOncol Biol Phys 2000;47:779-84. (Pubitemid 30317499)
46. Olive PL, Banath JP. Phosphorylation of histone H2AX as a measure of radiosensitivity. Int J Radiat Oncol Biol Phys 2004;58:331-5. (Pubitemid 38142456)
47. Genesca A, Martin M, Latre L, Soler D, Pampalona J, Tusell L. Telomere dysfunction: a new player in radiation sensitivity. Bioessays 2006;28:1172-80. (Pubitemid 44925437)
48. Shinomiya N. New concepts in radiation-induced apoptosis: 'premitotic apoptosis' and 'postmitotic apoptosis'. J Cell Mol Med 2001;5:240-53.
49. Lopez KA, Waziri AE, Canoll PD, Bruce JN. Convection-enhanced delivery in the treatment of malignant glioma. Neurol Res 2006;28:542-8. (Pubitemid 44141325)
50. Huppert JL, Balasubramanian S. G-quadruplexes in promoters throughout the human genome. Nucleic Acids Res 2007;35:406-13. (Pubitemid 46232058)