The alkylating carcinogen N-methyl-N′-nitro-N-nitrosoguanidine activates the plasminogen activator inhibitor-1 gene through sequential phosphorylation of p53 by ATM and ATR kinases

Thrombosis and Haemostasis

Volumn 93, Issue 3, 2005, Pages 584-591

  Vidal, Berta ^a   Parra, Maribel ^a   Jardí, Mercè ^a   Saito, Shin'ichi ^b   Appella, Ettore ^b   Muñoz Cánoves, Pura ^a  

^a CENTRE FOR GENOMIC REGULATION CRG   (Spain)

^b NATIONAL CANCER INSTITUTE   (United States)

Author keywords

Gene expression; Proteases inhibitors; Signal transduction

Indexed keywords

ATM PROTEIN; ATR PROTEIN; CAFFEINE; CHECKPOINT KINASE 1; CHECKPOINT KINASE 2; METHYLNITRONITROSOGUANIDINE; PLASMINOGEN ACTIVATOR INHIBITOR 1; PROTEIN P53;

ANIMAL CELL; APOPTOSIS; ARTICLE; CANCER CELL CULTURE; CELL DEATH; CELL SURVIVAL; CONTROLLED STUDY; ENZYME MECHANISM; ENZYME PHOSPHORYLATION; GENE EXPRESSION; GENETIC TRANSCRIPTION; IMMUNOFLUORESCENCE; MOLECULAR MECHANICS; MOUSE; NONHUMAN; PRIORITY JOURNAL; RNA EXTRACTION; WESTERN BLOTTING;

3T3 CELLS; ALKYLATING AGENTS; ANIMALS; CAFFEINE; CARCINOGENS; CELL CYCLE PROTEINS; CELL DEATH; DNA-ACTIVATED PROTEIN KINASE; DNA-BINDING PROTEINS; HUMANS; METHYLNITRONITROSOGUANIDINE; MICE; MICE, KNOCKOUT; NUCLEAR PROTEINS; PHOSPHORYLATION; PLASMINOGEN ACTIVATOR INHIBITOR 1; PROTEIN-SERINE-THREONINE KINASES; TRANSCRIPTIONAL ACTIVATION; TRANSFECTION; TUMOR SUPPRESSOR PROTEIN P53; TUMOR SUPPRESSOR PROTEINS;

EID: 15344348695     PISSN: 03406245     EISSN: None     Source Type: Journal    
DOI: 10.1160/TH04-10-0644     Document Type: Article

References (44)

1. Adamson AW, Kim WJ, Shangary S, et al. ATM is activated in response to N-methyl-N′-nitro-N-nitro-soguanidine-induced DNA alkylation. J Biol Chem 2002; 277: 38222-9.
2. Appella E, Anderson CW. Post-translational modifications and activation of p53 by genotoxic stresses. Eur J Biochem 2001; 268: 2764-72.
3. Banin S, Moyal L, Shieh S, et al. Enhanced phosphorylation of p53 by ATM in response to DNA damage. Science 1998; 281: 1674-7.
4. Block WD, Merkle D, Meek K, et al. Selective inhibition of the DNA-dependent protein kinase (DNA-PK) by the radiosensitizing agent caffeine. Nucleic Acids Res 2004; 32: 1967-72.
5. Brown KD, Ziv Y, Sadanandan SN, et al. The ataxia-telangiectasia gene product, a constitutively expressed nuclear protein that is not up-regulated following genome damage. Proc Natl Acad Sci U S A 1997; 94: 1840-5.
6. Canman CE, Lim DS, Cimprich KA, et al. Activation of the ATM kinase by ionizing radiation and phosphorylation of p53. Science 1998; 281: 1677-9.
7. Carmeliet P, Kieckens L, Schoonjans L, et al. Plasminogen activator inhibitor-1 gene-deficient mice. J Clin Invest 1993; 92: 2746-55.
8. Dunkern T, Roos W, Kaina B. Apoptosis induced by MNNG in human TK6 lymphoblastoid cells is p53 and Fas/CD95/Apo-1 related. Mutat Res 2003; 544: 167-72.
9. Eadie JS, Conrad M, Toorchen D, et al. Mechanism of mutagenesis by O6-methylguanine. Nature 1984; 308: 201-3.
10. Frisch SM, Screaton RA. Anoikis mechanisms. Curr Opin Cell Biol 2001; 13: 555-62.
11. Giaccia AJ, Kastan MB. The complexity of p53 modulation: emerging patterns from divergent signals. Genes Dev 1998; 12: 2973-83.
12. Griswold DP, Corbett TH. A colon tumor model for anticancer agent evaluation. Cancer 1975; 36: 2441-4.
13. Irigoyen JP, Munoz-Canoves P, Montero L, et al. The plasminogen activator system: biology and regulation. Cell Mol Life Sci 1999; 56: 104-32.
14. Jimenez GS, Bryntesson F, Torres-Arzayus MI, et al. DNA-dependent protein kinase is not required for the p53-dependent response to DNA damage. Nature 1999; 400: 81-3.
15. Kaina B, Fritz G, Mitra S, et al. Transfection and expression of human O6-methylguanine-DNAmethyl-transferase (MGMT) cDNA in Chinese hamster cells: the role of MGMT in protection against the genotoxic effects of alkylating agents. Carcinogenesis 1991; 12: 1857-67.
16. Keegan KS, Holtzman DA, Plug AW, et al. The Atr and Atm protein kinases associate with different sites along meiotically pairing chromosomes. Genes Dev 1996; 10: 2423-37.
17. Kleihues P, Margison GP. Carcinogenicity of N-methyl-N-nitrosourea: possible role of excision of O6-methylguanine from DNA. J Natl Cancer Inst 1974; 53: 1839-41.
18. Lees-Miller SP, Sakaguchi K, Ullrich SJ, et al. Human DNA-activated protein kinase phosphorylates serines 15 and 37 in the amino-terminal transactivation domain of human p53. Mol Cell Biol 1992; 12: 5041-9.
19. Levine AJ. p53, the cellular gatekeeper for growth and division. Cell 1997; 88: 323-31.
20. Lindstrom CG, Rosengren JE, Ekberg O. Experimental colonic tumours in the rat. III. Induction time, distribution and appearance of induced tumours. Acta Radiol Diagn 1978; 19: 799-816.
21. Loveless A. Possible relevance of O-6 alkylation of deoxyguanosine to the mutagenicity and carcinogenicity of nitrosamines and nitrosamides. Nature 1969; 223: 206-7.
22. Munoz-Canoves P, Miralles F, Baiget M, et al. Inhibition of urokinase-type plasminogen activator (uPA) abrogates myogenesis in vitro. Thromb Haemost 1997; 77: 526-34.
23. Nghiem P, Park PK, Kim YS, et al. ATR is not required for p53 activation but synergizes with p53 in the replication checkpoint. J Biol Chem 2002; 277: 4428-34.
24. Oren M. Regulation of the p53 tumor suppressor protein. J Biol Chem 1999; 274: 36031-4.
25. Parra M, Jardi M, Koziczak M, et al. p53 Phosphorylation at serine 15 is required for transcriptional induction of the plasminogen activator inhibitor-1 (PAI-1) gene by the alkylating agent N-methyl-N′-nitro-N-nitrosoguanidine. J Biol Chem 2001; 276: 36303-10.
26. Peto R, Gray R, Brantom R, et al. N-nitroso compounds: occurrence, biological effects and relevance to human cancer. IARC Scientific Publication no 57. International Agency for Research on Cancer, Lyon 1985; 627-55.
27. Prives C, Hall PA. The p53 pathway. J Pathol 1999; 187: 112-26.
28. Rotman G, Shiloh Y. ATM: a mediator of multiple responses to genotoxic stress. Oncogene 1999; 18: 6135-44.
29. Saffhill R, Margison GP, O'Connor PJ. Mechanisms of carcinogenesis induced by alkylating agents. Biochimica et Biophysica Acta 1985; 823: 111-45.
30. Saito S, Goodarzi AA, Higashimoto Y, et al. ATM mediates phosphorylation at multiple p53 sites, including Ser(46), in response to ionizing radiation. J Biol Chem 2002; 277: 12491-4.
31. Sakaguchi K, Herrera JE, Saito S, et al. DNA damage activates p53 through a phosphorylation-acetylation cascade. Genes Dev 1998; 12: 2831-41.
32. Sanchez-Prieto R, Rojas JM, Taya Y, et al. A role for the p38 mitogen-acitvated protein kinase pathway in the transcriptional activation of p53 on genotoxic stress by chemotherapeutic agents. Cancer Res 2000; 60: 2464-72.
33. Sarkaria JN, Busby EC, Tibbetts RS, et al. Inhibition of ATM and ATR kinase activities by the radiosensitizing agent, caffeine. Cancer Res 1999; 59: 4375-82.
34. Shulman LN. The biology of alkylating-agent cellular injury. Hematol Oncol Clin North Am 1993; 7: 325-35.
35. Siliciano JD, Cancan CE, Taya Y, et al. DNA damage induces phosphorylation of the amino terminus of p53. Genes Dev 1997; 11: 3471-81.
36. Singer B. The chemical effects of nucleic acids alkylation and their relation to mutagenesis and carcinogenesis. Prog Nucleic Acid Res 1975; 15: 219-84.
37. Singer B, Grunberger D. Molecular biology of mutagens and carcinogens. Plenum Press, New York 1983.
38. Thomale J, Huh NH, Nehls P, et al. Repair of O6-ethylguanine in DNA protects rat 208F cells fom tumorigenic conversion by N-ethyl-N-nitrosourea. Proc Natl Acad Sci U S A 1997; 87: 9883-7.
39. 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.
40. Tsujii M, Kawano S, Tsuji S, et al. Mechanism for ammonia-induced promotion of gastric carcinogenesis in rats. Carcinogenesis 1995; 16: 563-6.
41. Wesierska-Gadek J, Gueorguieva M, Schloffer D, et al. Non-apoptogenic killing of hela cervical carcinoma cells after short exposure to the alkylating agent N-methyl-N′-nitro-N-nitrosoguanidine (MNNG). J Cell Biochem 2003; 89: 1222-34.
42. Ye R, Bodero A, Zhou BB, et al. The plant isoflavenoid, genistein, activates p53 and Chk2 in an ATM-dependent manner. J Biol Chem 2000; 28: 28.
43. Yih LH, Lee TC. Arsenite induces p53 accumulation through an ATM-dependent pathway in human fibroblasts. Cancer Res 2000; 60: 6346-52.
44. Zhang Y, Ma WY, Kaji A, et al. Requirement of ATM in UVA-induced signaling and apoptosis. J Biol Chem 2002; 277: 3124-31.