Irinotecan activates p53 with its active metabolite, resulting in human hepatocellular carcinoma apoptosis

Journal of Pharmacological Sciences

Volumn 104, Issue 3, 2007, Pages 232-242

  Takeba, Yuko ^a   Kumai, Toshio ^a   Matsumoto, Naoki ^a   Nakaya, Sachiko ^a   Tsuzuki, Yoshimitsu ^a   Yanagida, Yohei ^a   Kobayashi, Shinichi ^a  

^a ST MARIANNA UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

Apoptosis; Huh7 cell; Irinotecan; p53 gene; SN 38

Indexed keywords

7 ETHYL 10 HYDROXYCAMPTOTHECIN; ANTISENSE OLIGONUCLEOTIDE; CASPASE 3; CASPASE 9; IRINOTECAN; PROTEIN BAX; PROTEIN BCL XL; PROTEIN P53; SERINE;

APOPTOSIS; ARTICLE; CELL CULTURE; CELL NUCLEUS; CELL PROLIFERATION; CELL STRAIN HEPG2; CONTROLLED STUDY; DRUG BINDING; GEL MOBILITY SHIFT ASSAY; HUMAN; HUMAN CELL; LIVER CELL CARCINOMA; METABOLITE; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; UPREGULATION;

EID: 34547202510     PISSN: 13478613     EISSN: 13478648     Source Type: Journal    
DOI: 10.1254/jphs.FP0070442     Document Type: Article

References (45)

1. Okuda K. Hepatocellular carcinoma. J Hepatol. 2000;32:225-237.
2. Bergsland EK. Molecular mechanisms underlying the development of hepatocellular carcinoma. Semin Oncol. 2001;28:521-531.
3. Shihabi S, Belani CP. Role of topoisomerase I inhibitors in small-cell lung cancer. Clin Lung Cancer. 2001;2:275-281.
4. Kim R, Hirabayashi N, Nishiyama M, Jinushi K, Toge T, Okada K. Experimental studies on biochemical modulation targeting topoisomerase I and II in human tumor xenografts in nude mice. Intl J Cancer. 1992;50:760-766.
5. Lansiaux A, Bras-Goncalves RA, Rosty C, Laurent-Puig P, Poupon MF, Bailly C. Topoisomerase I-DNA covalent complexes in human colorectal cancer xenografts with different p53 and microsatellite instability status: relation with their sensitivity to CTP-11. Anticancer Res. 2001;21:471-476.
6. Whitacre CM, Zborowska E, Willson JK, Berger NA. Detection of poly (ADP-ribose) polymerase cleavage in response to treatment with topoisomerase I inhibitors: a potential surrogate end point to assess. Clin Cancer Res. 1999;5:665-672.
7. Kawato Y, Aonuma M, Hirota Y, Kuga H, Sato K. Intracellular roles of SN-38, a metabolite of the camptothecin derivative CPT-11, in the antitumor effect of CPT-11. Cancer Res. 1991;51:4187-4191.
8. Rougier P, Van Cutsem E, Bajetta E, Niederle N, Possinger K, Labianca R, et al. Randomized trial of irinotecan versus fluorouracil by continuous infusion after fluorouracil failure in patients with metastatic colorectal cancer. Lancet. 1998;352:1407-1412.
9. Ueno M, Nonaka S, Yamazaki R, Deguchi N, Murai M. SN-38 induces cell cycle arrest and apoptosis in human testicular cancer. Eur Urol. 2002;42:390-397.
10. Levine AJ, Momand J, Finlay CA. The p53 tumor suppressor gene. Nature. 1991;351:453-456.
11. Lakin ND, Jackson SP. Regulation of p53 in response to DNA damage. Oncogene. 1999;18:7644-7655.
12. Abraham J, Kelly J, Thibault P, Benchimol S. Post-translational modification of p53 protein in response to ionizing radiation analyzed by mass spectrometry. J Mol Biol. 2000;295:853-864.
13. Wang S, El-Deiry WS. Requirement of p53 targets in chemosensitization of colonic carcinoma to death ligand therapy. Proc Natl Acad Sci U S A. 2003;100:15095-15100.
14. Koike M, Fujita F, Komori K, Katoh F, Sugimoto T, Sakamoto Y, et al. Dependence of chemotherapy response on p53 mutation status in a panel of human cancer lines maintained in nude mice. Cancer Sci. 2004;95:541-546.
15. Muller M, Strand S, Hug H, Heinemann EM, Walczak H, Hofmann WJ, et al. Drug-induced apoptosis in hepatoma cells is mediated by the CD95 (APO-1/Fas) receptor /ligand system and involves activation of wild-type p53. J Clin Invest. 1997;99:403-413.
16. LeBlanc H, Lawrence D, Varfolomeev E, Totpal K, Morlan J, Schow P, et al. Tumor-cell resistance to death receptor-induced apoptosis through mutational inactivation of the proapoptotic Bcl-2 homolog Bax. Nat Med. 2002;8:274-281.
17. Nakabayashi H, Taketa K, Miyano K, Yamane T, Sato J. Growth of human hepatoma cells lines with differentiated functions in chemically defined medium. Cancer Res. 1982;42:3858-3863.
18. Lin Y, Ong LK, Chan SH. Differential in situ hybridization of mutational specific expression of the p53 gene in human hepatoma cell lines. Pathology. 1995;27:191-196.
19. Scheithauer W, Clark GM, Salmon SE, Dorda, W, Shoemaker RH, Von Hoff DD. Model for estimation of clinically achievable plasma concentrations for investigational anticancer drugs in man. Cancer Treat Rep. 1986;70:1379-1382.
20. Kehrer DF, Yamamoto W, Verweij J, de Jonge MJ, de Bruijn, P, Sparreboom A. Factors involved in prolongation of terminal disposition phase of SN-38:clinical and experimental studies. Clin Cancer Res. 2000;6:3451-3458.
21. Taniguchi R, Kumai T, Matsumoto N, Watanabe M, Kamio K, Suzuki S, et al. Utilization of human liver microsomes to explain individual differences in paclitaxel metabolism by CYP2C8 and CYP3A4. J Pharmacol Sci. 2005;97:83-90.
22. Isenoumi K, Kumai T, Kitaoka Y, Motoki M, Kitaoka Y, Kuribayashi K, et al. N-methyl-D-aspartate induces phosphorylation of cAMP response element (CRE)-binding protein and increases DNA-binding activity of CRE in rat retina. J Pharmacol Sci. 2004;95:108-114.
23. Jiang C, Hu H, Malewicz B, Wang Z, Lu J. Selenite-induced p53 Ser-15 phosphorylation and caspase-mediated apoptosis in LNCaP human prostate cancer cells. Mol Cancer Ther. 2004;3:877-884.
24. Katiyar SK, Roy AM, Baliga MS. Silymarin induces apoptosis primarily through a p53-dependent pathway involving Bcl-2 /Bax, cytochrome c release, and caspase activation. Mol Cancer Ther. 2005;4:207-216.
25. Kanazawa F, Sugimoto Y, Minato K, Kasahara K, Bungo M, Nakazawa K, et al. Establishment of a camptothecin analogue (CPT-11)-resistant cell line of human non-small cell lung cancer: characterization and mechanism of resistance. Cancer Res. 1990;50:5919-5924.
26. Jansen WJ, Zwart B, Hulscher ST, Giaccone G, Pinedo HM, Boven E. CPT-11 in colon-cancer cell lines and xenografts: characterization of cellular sensitivity determinants. Int J Cancer. 1997;70:335-340.
27. Harris CC. p53: at the crossroads of molecular carcinogenesis and risk assessment. Science. 1993;262:1980-1981.
28. Oshita F, Nishio K, Kameda Y, Mitsuda A, Ikehara M, Tanaka G, et al. Increased expression levels of p53 correlate with good response to cisplatin-based chemotherapy in non-small cell lung cancer. Oncol Rep. 2000;7:1225-1228.
29. Boyer J, McLean EG, Aroori S, Wilson P, McCulla A, Carey PD, et al. Characterization of p53 wild-type and null isogenic colorectal cancer cell lines resistant to 5-fluorouracil, oxaliplatin, and irinotecan. Clin Cancer Res. 2004;10:2158-2167.
30. Shieh SY, Ikeda M, Taya Y, Prives C. DNA damage-induced phosphorylation of p53 alleviates inhibition by MDM2. Cell. 1997;91:325-334.
31. Siliciano JD, Canman CE, Taya Y, Sakaguchi K, Appella E, Kastan MB. DNA damage induces phosphorylation of the amino terminus of p53. Genes Dev. 1997;11:3471-3481.
32. Lowe SW, Ruley HE, Jacks T, Housman DE. p53-dependent modulates the cytotoxicity of anticancer agents. Cell. 1993;74:957-967.
33. Magrini R, Bhonde MR, Hanski ML, Notter M, Scherubl H, Boland CR, et al. Cellular effects of CPT-11 on colon carcinoma cells: dependence on p53 and hMLH1 status. Int J Cancer. 2002;101:23-31.
34. Green DR, Reed JC. Mitochondria and apoptosis. Science. 1998;281:1309-1312.
35. Korsmeyer SJ. BCL-2 gene family and the regulation of programmed cell death. Cancer Res. 1999;59:1693s-1700s.
36. Zhan Q, Fan S, Bae I, Guillouf C, Liebermann DA, O'Connor PM, et al. Induction of bax by genotoxic stress in human cells correlates with normal p53 status and apoptosis. Oncogene. 1994;9:3743-3751.
37. Yu J, Zhang L, Hwang PM, Rago C, Kinzler KW, Vogelstein B. Identification and classification of p53-regulated genes. Proc Nat Acad Sci U S A. 1999;96:14517-14522.
38. Zhang L, Yu J, Park BH, Kinzler KW, Vogelstein B. Role of BAX in the apoptotic response to anticancer agents. Science. 2000;290:989-992.
39. Ionov Y, Yamamoto H, Krajewski S, Reed JC, Perucho M. Mutational inactivation of the proapoptotic gene BAX confers selective advantage during tumor clonal evolution. Proc Natl Acad Sci U S A. 2000;97:10872-10877.
40. Hayward RL, Macpherson JS, Cummings J, Monia BP, Smyth JF, Jodrell DI. Antisense Bcl-xl down-regulation switches the response to topoisomerase I inhibition from senescence to apoptosis in colorectal cancer cells, enhancing global cytotoxicity. Cancer Res. 2003;9:2856-2865.
41. Takehara T, Liu X, Fujimoto J, Friedman SL, Takahashi H. Expression and role of Bcl-xl in human hepatocellular carcinomas. Hepatol. 2001;34:55-61.
42. Denault JB, Salvesen GS. Caspase: keys in the ignition of cell death. Chem Rev. 2002;102:4489-4500.
43. Soengas MS, Alarcon RM, Yoshida H, Giaccia AJ, Hakem R, Mak T, et al. Apaf-1 and caspase-9 in p53-depandent apoptosis and tumor inhibition. Science. 1999;284;156-159.
44. Gualdi R, Bossard P, Zheng M, Hamada Y, Coleman JR, Zaret KS. Hepatic specification of the gut endoderm in vitro: cell signaling and transcriptional control. Genes Dev. 1996;10:1670-1682.
45. Keramaris E, Hirao A, Slack RS, Mak TW, Park DS. Ataxia telangiectasia-mutated protein can regulate p53 and neuronal death independent of Chk2 in response to DNA damage. J Biol Chem. 2003;278:37782-37789.