Identification and characterization of a novel and specific inhibitor of the ataxia-telangiectasia mutated kinase ATM

Cancer Research

Volumn 64, Issue 24, 2004, Pages 9152-9159

  Hickson, Ian ^a   Zhao, Yan ^b   Richardson, Caroline J ^a   Green, Sharon J ^a   Martin, Niall M B ^a   Orr, Alisdair I ^a   Reaper, Philip M ^c   Jackson, Stephen P ^c   Curtin, Nicola J ^b   Smith, Graeme C M ^a  

^a KuDOS Pharmaceuticals Ltd   (United Kingdom)

^b NEWCASTLE UNIVERSITY   (United Kingdom)

^c UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

2 MORPHOLIN 4 YL 6 THIANTHREN 1 YL PYRAN 4 ONE; BRCA1 PROTEIN; CAMPTOTHECIN; CHECKPOINT KINASE 2; DOUBLE STRANDED DNA; DOXORUBICIN; ETOPOSIDE; GAMMAH2AX PROTEIN; KU 55933; KU 58050; NIBRIN; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN; PROTEIN P53; PROTEIN SERINE THREONINE KINASE; SMC1 PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; ATAXIA TELANGIECTASIA; ATM GENE; AUTOSOMAL RECESSIVE DISORDER; CELL CYCLE; COMPETITIVE INHIBITION; CONTROLLED STUDY; CYTOTOXICITY; DNA DAMAGE; DNA REPAIR; DNA STRAND BREAKAGE; DRUG EFFECT; ENZYME ASSAY; ENZYME KINETICS; GENE; GENE MUTATION; GENETIC ANALYSIS; GENETIC IDENTIFICATION; HUMAN; HUMAN CELL; IC 50; IONIZING RADIATION; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RADIOSENSITIVITY; SIGNAL TRANSDUCTION; ULTRAVIOLET RADIATION;

CELL CYCLE; CELL CYCLE PROTEINS; CELL LINE, TUMOR; CHROMONES; COMBINATORIAL CHEMISTRY TECHNIQUES; DNA-BINDING PROTEINS; HELA CELLS; HUMANS; INHIBITORY CONCENTRATION 50; KINETICS; MORPHOLINES; PHOSPHORYLATION; PROTEIN KINASE INHIBITORS; PROTEIN-SERINE-THREONINE KINASES; PYRONES; RADIATION-SENSITIZING AGENTS; TUMOR SUPPRESSOR PROTEINS;

EID: 9744271049     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-04-2727     Document Type: Article

References (57)

1. Rouse J, Jackson SP. Interfaces between the detection, signaling and repair of DNA damage. Science (Wash. DC) 2002;297:547-51.
2. Zakian VA. ATM-related genes: what do they tell us about functions of the human gene? Cell 1995;82:685-7.
3. Abraham RT. Cell cycle checkpoint signaling through the ATM and ATR kinases. Genes Dev 2001;15:2177-96.
4. Shiloh Y. ATM and related protein kinases: safeguarding genome integrity. Nat Cancer Rev 2003;3:155-68.
5. Lavin MF, Shiloh Y. The genetic defect in ataxia-telangiectasia. Annu Rev Immunol 1997;15:177-202.
6. Rotman G, Shiloh Y. ATM from gene to function. Hum Mol Genet 1988;7:1555-63.
7. Kastan MB, Lim DS. The many substrates and functions of ATM. Nat Rev Mol Cell Biol 2000;1:179-86.
8. Shiloh Y. ATM and ATR: networking cellular responses to DNA damage. Curr Opin Genet Dev 2001;11:71-7.
9. 2-M checkpoints are induced by ionizing irradiation. Mol Cell Biol 2002;22:1049-59.
10. Canman CE, Lim DS, Cimprich KA, et al. Activation of the ATM kinase by ionizing radiation and phosphorylation of p53. Science (Wash. DC) 1988;281:1677-9.
11. Banin S, Moyal L, Shieh S, et al. Enhanced phosphorylation of p53 by ATM in response to DNA damage. Science (Wash. DC) 1998;281:1674-7.
12. Matsuoka S, Rotman G, Ogawa A, Shiloh Y, Tamai K, Elledge SJ. Ataxia telangiectasia-mutated phosphorylates Chk2 in vivo and in vitro. Proc Natl Acad Sci 2000;97:10389-94.
13. Maya R, Balass M, Kim ST, et al. ATM-dependent phosphorylation of Mdm2 on serine 395: role in p53 activation by DNA damage. Genes Dev 1999;15:1067-77.
14. Zhao S, Weng YC, Yuan SS, et al. Functional link between ataxia-telangiectasia and Nijmegen breakage syndrome gene products. Nature (Lond.) 2000;405:473-7.
15. Bao S, Tibbetts RS, Brumbaugh KM, et al. ATR/ATM-mediated phosphorylation of human Rad 17 is required for genotoxic stress responses. Nature (Lond.) 2001;411:969-74.
16. 2-phase checkpoints after ionizing irradiation. Mol Cell Biol 2001;21:3445-50.
17. Fornace AL Jr, Little JB. Normal repair of DNA single-strand breaks in patients with ataxia-telangiectasia. Biochem Biophys Acta 1980;607:432-7.
18. Lavin MF, Davidson M. Repair of strand breaks in superhelical DNA of ataxia-telangiectasia lymphoblastoid cells. J Cell Sci 1981;48:383-91.
19. Cornforth MN, Bedford JS. On the nature of a defect in cells from individuals with ataxia-telangiectasia. Science (Wash. DC) 1985;227:1589-91.
20. 241Am alpha-particles or bleomycin. Int J Radiat Biol Relat Stud Phys Chem Med 1987;51:209-18.
21. Foray N, Priestley A, Alsbeih G, et al. Hypersensitivity of ataxia-telangiectasia fibroblasts to ionizing radiation is associated with a repair deficiency of DNA double-strand breaks. Int J Radiat Biol 1997;72:271-83.
22. Sarkaria JN, Eshleman JS. ATM as a target for novel radiosensitizers. Semin Radiat Oncol 2001;11:316-27.
23. Sarkaria JN, Tibbetts RS, Busby EC, Kennedy AP, Hill DE, Abraham RT. Inhibition of phosphoinositide 3-kinase related kinases by the radiosensitizing agent wortmannin. Cancer Res 1998;58:4375-82.
24. Izzard RA, Jackson SP, Smith GCM. Competitive and non-competitive inhibition of the DNA dependent protein kinase. Cancer Res 1999;59:2581-6.
25. Ui M, Okada T, Hazeki K, Hazeki O. Wortmannin as a unique probe for an intracellular signalling protein, phosphoinositide 3-kinase. Trends Biochem Sci 1995;20:303-7.
26. 2-M DNA damage checkpoint by inhibiting ataxia-telangiectasia-mutated kinase activity. J Biol Chem 2000;5:10342-8.
27. Block WD, Merkle D, Meek K, Lees-Miller SP. Selective inhibition of the DNA-dependent protein kinase (DNA-PK) by the radiosensitizing agent caffeine. Nucleic Acid Res 2004;32:1967-72.
28. Vlahos CJ, Matter WF, Hui KY, Brown RF. A specific inhibitor of phosphatidylinositol 3-kinase, 2-(4-morpholinyl)-8-phenyl-4H-1-benzopyran-4-one (LY294002). J Biol Chem 1994;269:5241-8.
29. Blunt T, Finnic NJ, Taccioli GE, et al. Defective DNA-dependent protein kinase activity is linked to V(D)J recombination and DNA repair defects associated with the murine scid mutation. Cell 1995;80:813-23.
30. Tibbetts RS, Brumbaugh KM, Williams JM, et al. A role for ATR in the DNA damage-induced phosphorylation of p53. Genes Dev 1999;13:152-7.
31. Brunn GJ, Williams J, Sabers C, Wiederrecht G, Lawrence JC, Abraham RT. Direct inhibition of the signaling functions of the mammalian target of rapamycin by the phosphoinositide 3-kinase inhibitors, wortmannin and LY294002. EMBO J 1996;15:5256-67.
32. Veuger SJ, Curtin NJ, Richardson CJ, Smith GCM, Durkacz BW. Radiosensitization and DNA repair inhibition by the combined use of novel inhibitors of DNA-dependent protein kinase and poly (ADP-ribose) polymerase-1. Cancer Res 2003;63:6008-15.
33. Zhao X-H, Bondeva T, Balla T. Characterization of recombinant phosphatidylinositol 4-kinase beta reveals auto- and heterophosphorylation of the enzyme. J Biol Chem 2000;275:14642-8.
34. Allan LA, Fried M. p53-dependent apoptosis or growth arrest induced by different forms of radiation in U2OS cells: p21WAF1/CIP1 repression in UV induced apoptosis. Oncogene 1999;18:5403-12.
35. Ormerod MG. Analysis of DNA-general methods. In: Ormerod MG, editor. Flow cytometry. Oxford, UK: Oxford University Press; 2000. p. 83-97.
36. Walker EH, Pacold ME, Perisic O, et al. Structural determinants of phosphoinositide 3-kinase inhibition by wortmannin, LY294002, quercetin, myricetin, and staurosporine. Mol Cell 2000;6:909-19.
37. Burma S, Chen BP, Murphy M, Kurimasa A, Chen DJ. ATM phosphorylates histone H2AX in response to DNA double-strand breaks. J Biol Chem 2001;276:42462-7.
38. Lim DS, Kim ST, Xu B, et al. ATM phosphorylates p95/nbs1 in an S-phase checkpoint pathway. Nature (Lond.) 2000;404:613-7.
39. 2-M DNA damage checkpoint. Genes Dev 2000;14:1448-59.
40. Kim ST, Xu B, Kastan MB. Involvement of the cohesin protein, Smc1, in Atm-dependent and independent responses to DNA damage. Genes Dev 2002;16:560-70.
41. Caporossi D, Porfirio B, Nicoletti B, et al. Hypersensitivity of lymphoblastoid lines derived from ataxia-telangiectasia patients to the induction of chromosomal aberrations by etoposide (VP-16). Mutat Res 1993;290:265-72.
42. Henner WD, Blazka ME. Hypersensitivity of cultured ataxia-telangiectasia cells to etoposide. J Natl Cancer Inst (Bethesda) 1986;76:1007-11.
43. Fedier A, Schlamminger M, Schwarz VA, Haller U, Howell SB, Fink D. Loss of atm sensitises p53-deficient cells to topoisomerase poisons and antimetabolites. Ann Oncol 2003;14:938-45.
44. 1 cell cycle checkpoint pathway and ataxia-telangiectasia. Cancer Res 1994;54:5054-8.
45. Chehab NH, Malikzay A, Stavridi ES, Halazonetis TD. Phosphorylation of Ser-20 mediates stabilization of human p53 in response to DNA damage. Proc Natl Acad Sci USA 1999;96:13777-82.
46. Stiff T, O'Driscoll M, Rief N, Iwabuchi K, Lobrich M, Jeggo PA. ATM and DNA-PK function redundantly to phosphorylate H2AX after exposure to ionizing radiation. Cancer Res 2004;64:2390-6.
47. Bakkenist CJ, Kastan MB. DNA damage activates ATM through intermolecular autophosphorylation and dimer dissociation. Nature (Lond.) 2003;421:499-506.
48. Gosink EC, Chong MJ, McKinnon PJ. Ataxia-telangiectasia mutated deficiency affects astrocyte growth but not radiosensitivity. Cancer Res 1999;59:5294-8.
49. Takimoto CH, Arbuck SG. Topoisomerase I targeting agents: the camptothecins. In: Chabner BA, Longo DL, editors. Cancer chemotherapy and biotherapy: principles and practice. Philadelphia: Lippincott, Williams and Wilkins; 2001. p. 579-646.
50. Smith PJ, Makinson TA, Watson JV. Enhanced sensitivity to camptothecin in ataxia-telangiectasia cells and its relationship with the expression of DNA topoisomerase I. Int J Radiat Biol 1989;55:217-31.
51. Pommier YG, Goldwasser F and Strumberg D. Topoisomerase II inhibitors: epipodophyllotoxins, acridines, ellipticines, and bisdioxopiperazines. In: Chabner BA, Longo DL, editors. Cancer chemotherapy and biotherapy: principles and practice. Philadelphia: Lippincott, Williams & Wilkins; 2001. p. 538-78.
52. 6-methylguanine repair in human normal and ataxia-telangiectasia cell lines and correlation of repair capacity with cellular sensitivity to methylating agents. Cancer Res 1981;41:5114-20.
53. Jaspers NG, de Wit J, Regulski MR, Bootsma D. Abnormal regulation of DNA replication and increased lethality in ataxia-telangiectasia cells exposed to carcinogenic agents. Cancer Res 1982;42:335-41.
54. Zhang N, Chen P, Gatei M, Scott S, Khanna KK, Lavin MF. An anti-sense construct of full-length ATM cDNA imposes a radiosensitive phenotype on normal cells. Oncogene 1998;17:811-8.
55. Uhrhammer N, Fritz E, Boyden L, Meyn MS. Human fibrobiasts transfected with an ATM antisense vector respond abnormally to ionizing radiation. Int J Mol Med 1999;4:43-7.
56. Guha C, Guha U, Tribius S, et al. Antisense ATM gene therapy: a strategy to increase the radiosensitivity of human tumors. Gene Ther 2000;7:852-8.
57. Collis SJ, Swartz MJ, Nelson WG, DeWeese TL. Enhanced radiation and chemotherapy-mediated cell killing of human cancer cells by small inhibitory RNA silencing of DNA repair factors. Cancer Res 2003;63:1550-4.