The irinotecan/5-fluorouracil combination induces apoptosis and enhances manganese superoxide dismutase activity in HT-29 human colon carcinoma cells

Chemotherapy

Volumn 51, Issue 2-3, 2005, Pages 93-102

  Grivicich, Ivana ^a,b,c   Regner, Andréa ^b   Da Rocha, Adriana B ^b   Kayser, Guilherme B ^b   Schunemann, Daniel P ^b   Grass, Luciano B ^b   Alves, Pedro A G ^b   Henriques, João A P ^b,c   Schwartsmann, Gilberto ^a,c  

^a South American Office for Anticancer Drug Development SOAD   (Brazil)

^b UNIVERSIDADE LUTERANA DO BRASIL   (Brazil)

^c FEDERAL UNIVERSITY OF RIO GRANDE DO SUL   (Brazil)

Author keywords

Apoptosis; CPT 11 5 FU combination; HT 29 human colon carcinoma cells; Mn SOD activity

Indexed keywords

COPPER ZINC SUPEROXIDE DISMUTASE; FLUOROURACIL; IRINOTECAN; MANGANESE SUPEROXIDE DISMUTASE;

APOPTOSIS; ARTICLE; CANCER CELL; COLON CARCINOMA; CONTROLLED STUDY; DRUG EFFECT; ENZYME ACTIVITY; FLOW CYTOMETRY; HUMAN; HUMAN CELL; INTERMETHOD COMPARISON; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; STATISTICAL SIGNIFICANCE;

ANTINEOPLASTIC AGENTS; APOPTOSIS; CAMPTOTHECIN; COLONIC NEOPLASMS; DRUG SYNERGISM; ELECTROPHORESIS, POLYACRYLAMIDE GEL; FLOW CYTOMETRY; FLUOROURACIL; HT29 CELLS; HUMANS; SUPEROXIDE DISMUTASE;

EID: 22144463566     PISSN: 00093157     EISSN: None     Source Type: Journal    
DOI: 10.1159/000085617     Document Type: Article

References (67)

1. Benson AB III, Goldberg RM: Optimal use of the combination of irinotecan and 5-fluorouracil. Semin Oncol 2003;30(suppl 6):68-77.
2. Grivicich I, Mans DRA, Peters GJ, Schwartsmann G: Irinotecan and oxaliplatin: An overview of the novel chemotherapeutic options for the treatment of advanced colorectal cancer. Braz J Med Biol Res 2001;34:1087-1103.
3. Rougier P, Mitry E: Review of the role of CPT-11 in the treatment of colorectal cancer. Clin Colorectal Cancer 2001;1:87-94.
4. Pito HC, Wender DB, O'Connell MJ, Schroeder G, Goldberg RM, Rubin J, Maillard JA, Knost JA, Ghosh C, Kirschling RJ, Levitt R, Windschitl HE: Phase II trial of irinotecan in patients with metastatic colorectal carcinoma. J Clin Oncol 1997;15:2910-2919.
5. Saltz LB, Douillard J, Pirotta N, Alaki M, Gruia G, Awad L, Elfring GL, Locker PK, Miller LL: Irinotecan plus fluorouracil/LV for metastatic colorectal cancer: A new survival standard. Oncologist 2001;6:81-91.
6. Douillard JY, Cunningham D, Roth AD, Navarro M, James RD, Karasek P, Jandik P, Iveson T, Carmichael J, Alaki M, Gruia G, Awad L, Rougier P: Irinotecan combined with fluorouracil compared with fluorouracil alone as first-line treatment for metastatic colorectal cancer: A multicentre randomized trial. Lancet 2000;355:1041-1047.
7. Longley DB, Harkin DP, Johnston PG: 5-Fluorouracil: Mechanisms of action and clinical strategies. Natl Rev Cancer 2003;3:330-338.
8. Sobrero AF, Aschele C, Bertino JR: Fluorouracil in colorectal cancer - a tale of two drugs: Implications for biochemical modulation. J Clin Oncol 1997;15:368-381.
9. Tsavaris NB, Polyzos A, Gennatas K, Kosmas C, Vadiaka M, Dimitrakopoulos A, Macheras A, Papastratis G, Tsipras H, Margaris H, Papalambros E, Giannopoulos A, Koufos CH: Irinotecan (CPT-11) in patients with advanced colon carcinoma relapsing after 5-fluorouracil-leucovorin combination. Chemotherapy 2002;48:94-99.
10. Pizzolato JF, Saltz LB: The camptothecins. Lancet 2003;361:2235-2242.
11. Sanghani SP, Quinney SK, Fredenburg TB, Davis WI, Murry DJ, Bosron WF: Hydrolysis of irinotecan and its oxidative metabolites, 7-ethyl-10-[4-N-(5- aminopentanoic acid)-1-piperidino] carbonyloxycamptothecin and 7-ethyl-10-[4-(1-piperidino)-1-amino]-carbonyloxycamptothecin, by human carboxylesterases CES1A1, CES2, and a newly expressed carboxylesterase isoenzyme, CES3. Drug Metab Dispos 2004;32:505-511.
12. Guichard S, Cussac D, Hennebelle I, Bugat R, Canal P: Sequence-dependent activity of the irinotecan-5-FU combination in human colon-cancer model HT-29 in vitro and in vivo. Int J Cancer 1997;73:729-734.
13. Pavillard V, Formento P, Rostagno P, Formento JL, Fischel JL, Francoual M, Etienne MC, Milano G: Combination of irinotecan (CPT-11) and 5-fluorouracil with an analysis of cellular determinants of drug activity. Biochem Pharmacol 1998;56:1315-1322.
14. Mans DRA, Grivicich I, Peters GJ, Schwartsmann G: Sequence-dependent growth inhibition and DNA damage formation by the irinotecan-5-fluorouracil combination in human colon carcinoma cell lines. Eur J Cancer 1999;35:1851-1861.
15. Azrak RG, Cao S, Slocum HK, Toth K, Durrani FA, Yin MB, Pendyala L, Zhang W, McLeod HL, Rustum YM: Therapeutic synergy between irinotecan and 5-fluorouracil against human tumor xenografts. Clin Cancer Res 2004;10:1121-1129.
16. Peters GJ, van der Wilt CL, van Moorsel CJ, Kroep JR, Bergman AM, Ackland SP: Basis for effective combination cancer chemotherapy with antimetabolites. Pharmacol Ther 2000;87:227-253.
17. Ducreux M, Kohne CH, Schwartz GK, Vanhoefer U: Irinotecan in metastatic colorectal cancer: Dose intensification and combination with new agents, including biological response modifiers. Ann Oncol 2003;14(suppl 2):17-23.
18. Thornberry NA, Lazebnik Y: Caspases: Enemies within. Science 1998;281:1312-1316.
19. Schreck R, Rieber P, Bauerle PA: Reactive oxygen intermediates as apparently widely used messengers in the activation of NF-kappa B transcription factor and HIV-1. EMBO J 1991;10:2247-2258.
20. Rao GN: Hydrogen peroxide induces complex formation of SHC-Grb 2-SOS receptor tyrosine kinase and activates ras and extracellular signal related protein kinase group of mitogen activated protein kinases. Oncogenes 1996;13:713-719.
21. Bae YS, Kang SW, Seo MS, Baines IC, Tekle E, Chock P, Rhee SG: Epidermal Growth Factor (EGF)-induced generation of hydrogen peroxide. J Biol Chem 1997;272:217-221.
22. Irani K, Xia Y, Zweier JL, Sollot SJ, Der CJ, Fearon ER, Sundaresan M, Finkel T, Goldschmit-Clermont J: Mitogenic signaling mediatec by oxidants in ras-transformed fibroblasts. Science 1997;275:1649-1651.
23. Chung YM, Bae YS, Lee SY: Molecular ordering of ROS production, mitochondrial changes, and caspase activation during sodium salicylate-induced apoptosis. Free Radic Biol Med 2003;34:434-442.
24. Janssen YMW, Houten BV, Borm PJZ, Mossman BT: Cell and tissue responses to oxidative damage. Lab Invest 1993;69:261-274.
25. Hassan HM: Biosynthesis and regulation of superoxide dismutases. Free Radic Biol Med 1998;5:377-385.
26. Touati D: Molecular genetics of superoxide dismutases. Free Radic Biol Med 1988;5:393-402.
27. Hirose K, Longo DL, Oppenheim JJ, Matsushima K: Overexpression of mitochondrial manganese superoxide dismutase promotes the survival of tumor cells exposed to interleukin-1, tumor necrosis factor, selected anticancer drugs, and ionizing radiation. FASEB J 1993;7:361-368.
28. Li JJ, Oberley LW: Overexpression of manganese-containing superoxide dismutase confers resistance to the cytotoxicity of tumor necrosis factor alpha and/or hyperthermia. Cancer Res 1997;57:1991-1998.
29. Cullen JJ, Weydert C, Hinkhouse MM, Ritchie J, Domann FE, Spitz D, Oberley LW: The role of manganese superoxide dismutase in the growth of pancreatic adenocarcinoma. Cancer Res 2003;63:1297-1303.
30. Church SL, Grant JW, Ridnour LA, Oberley LW, Swanson PE, Meltzer PS, Trent JM: Increased manganese superoxide dismutase expression suppresses the malignant phenotype of human melanoma cells. Proc Natl Acad Sci USA 1993;90:3113-3117.
31. Zhang Y, Zhao W, Zhang HJ, Domann FE, Oberley LW: Overexpression of copper zinc superoxide dismutase suppresses human glioma cell growth. Cancer Res 2002;62:1205-1212.
32. Zhao Y, Xue Y, Oberley TD, Kiningham KK, Lin SM, Yen HC, Majima H, Hines J, St Clair D: Overexpression of manganese superoxide dismutase suppresses tumor formation by modulation of activator protein-1 signaling in a multistage skin carcinogenesis model. Cancer Res 2001;61:6082-6088.
33. Hussain SP, Amstad P, He P, Robles A, Lupold S, Kaneko I, Ichimiya M, Sengupta S, Mechanic L, Okamura S, Hofseth LJ, Moake M, Nagashima M, Forrester KS, Harris CC: p53-induced up-regulation of MnSOD and GPx but not catalase increases oxidative stress and apoptosis. Cancer Res 2004;64:2350-2356.
34. Cobbs CS, Levi DS, Aldape K, Israel MA: Manganese superoxide dismutase expression in human central nervous system tumours. Cancer Res 1996;56:3192-3195.
35. Kinnula VL, Pietarinen-Runtti P, Raivio K, Kahlos K, Pelin K, Mattson K, Linnainmaa K: Manganese superoxide dismutase in human pleural mesothelioma cell lines. Free Radical Biol Med 1996;21:527-532.
36. Landriscina M, Remiddi F, Ria F, Palazzotti B, De Leo ME, Iacoangeli M, Rosselli R, Scerrati M, Galeotti T: The level of MnSOD is directly correlated with grade of brain tumours of neuroepithelial origin. Br J Cancer 1996;74:1877-1885.
37. Janssen AML, Bosman CB, Sier CFM, Griffioen G, Kubben FJGM, Lamers CBHW, van Krieken JHJM, van de Veide CJH, Verspaget HW: Superoxide dismutases in relation to the overall survival of colorectal cancer patients. Br J Cancer 1998;78:1051-1057.
38. Skehan P, Storeng R, Scudiero D, Monks A, McMahon J, Vistica D, Warren JT, Bokesch H, Kenney S, Boyd MR: New colorimetric cytotoxicity assay for anticancer-drug screening. J Natl Cancer Inst 1990;13:1107-1112.
39. Chou T-C, Talahay P: Quantitative analysis of dose-effect relationship: The combined effects of multiple drugs on enzyme inhibitors; in Weber G (ed): Advances in Enzyme Regulation. New York, Pergamon Press, 1983, pp 27-55.
40. Nicoletti I, Migliorati G, Pagliacci MC, Grignani F, Riccardi C: A rapid and simple method for measuring thymocyte apoptosis by propidium iodide staining and flow cytometry. J Immunol Methods 1991;139:271-279.
41. Broquet P, Rodriguez-Lafrasse C, Alphonse G, Aloy MT, Louisot P, Rousson R: Comparison of methods used to study cell death in an adherent tumoral cell line with moderate clonogenic radiosensitivity. Neoplasma 2001;48:362-369.
42. Swe M, SRR KH: Z-VAD-fmk and DEVD-cho induced late mitosis arrest and apoptotic expressions. Apoptosis, 2000.
43. Laemmli UK: Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970;227:680-685.
44. Azevedo RA, Alas RM, Smith RJ, Lea PJ: Response of antioxidant enzymes to transfer from elevated carbon dioxide to air and ozone fumigation, in the leaves and roots of wild-type and a catalase-deficient mutant of barley. Physiol Plant 1998;104:280-292.
45. Bradford MM: A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 1976;72:248-254.
46. Andre T, de Gramont A: Study Group of Clinical Research in Radiotherapies Oncology, Oncology Multidiciplinary Research Group: An overview of adjuvant systemic chemotherapy for colon cancer. Clin Colorectal Cancer 2004;4(suppl 1):S22-S28.
47. Yang TS, Chen JS, Tang R, Chiang JM, Hsieh PS, Yen CY, Changchien CR: Oxaliplatin with weekly bolus 5-fluorouracil and leucovorin in pretreated advanced colorectal cancer patients: A phase II study. Chemotherapy 2003;49:194-199.
48. Fischer G, Kent SC, Joseph L, Green DR, Scott DW: Lymphoma models for B cell activation and tolerance. X. Anti-mu-mediated growth arrest and apoptosis of murine B cell lymphomas is prevented by the stabilization of myc. J Exp Med 1994;179:221-228.
49. Pommier Y, Sordet O, Antony S, Hayward RL, Kohn KW: Apoptosis defects and chemotherapy resistance: Molecular interaction maps and networks. Oncogene 2004;23:2934-2949.
50. Matsushima Y, Kanzawa F, Hoshi A, Shimizu E, Nomori H, Sasaki Y, Saijo N: Time-schedule dependency of the inhibiting activity of various anticancer drugs in the clonogenic assay. Cancer Chemother Pharmacol 1985;14:104-107.
51. Shackelford RE, Kaufmann WK, Paules RS: Cell cycle control, checkpoint mechanisms, and genotoxic stress. Environ Health Perspect 1999;107(suppl 1):5-24.
52. Gottlieb RA: Mitochondria and apoptosis. Biol Signals Recept 2001;10:147-161.
53. Lotem J, Peled-Kamar M, Groner Y, Sachs L: Cellular oxidative stress and the control of apoptosis by wild-type p53, cytotoxic compounds and cytokines. Proc Natl Acad Sci USA 1996;93:9166-9171.
54. Hwang PM, Bunz F, Yu J, Rago C, Chan TA, Murphy MP, Kelso GF, Smith RA, Kinzler KW, Vogelstein B: Ferredoxin reductase affects p53-dependent, 5-fluorouracil-induced apoptosis in colorectal cancer cells. Nat Med 2001;7:1111-1117.
55. Shimura M, Osawa Y, Yuo A, Hatake K, Takaku F, Ishizaka Y: Oxidative stress as a necessary factor in room temperature-induced apoptosis of HL-60 cells. J Leukoc Biol 2000;68:87-96.
56. L prevents the initial decrease in mitochondrial membrane potential and subsequent reactive oxygen species production during tumor necrosis factor alpha-induced apoptosis. Mol Cell Biol 2000;20:5680-5689.
57. Hiura TS, Li N, Kaplan R, Horwitz M, Seagrave JC, Nel AE: The role of a mitochondrial pathway in the induction of apoptosis by chemicals extracted from diesel exhaust particles. J Immunol 2000;165:2703-2711.
58. Tsujimoto Y, Simizu S: Bcl-2 family: life-or-death switch. FEBS Lett 2000;466:6-10.
59. Ueta E, Yoneda K, Kimura T, Tatemoto Y, Doi S, Yamamoto T, Osaki T: Mn-SOD antisense upregulates in vivo apoptosis of squamous cell carcinoma cells by anticancer drugs and γ-rays regulating expression of the bcl-2 family proteins, cox-2 and p21. Int J Cancer 2001;94:545-550.
60. Oberley TD, Oberley LW: Antioxidant enzyme levels in cancer. Histol Histopathol 1997;12:525-535.
61. Zhong W, Yan T, Webber MM, Oberley TD: Alteration of cellular phenotype and responses to oxidative stress by manganese superoxide dismutase and a superoxide dismutase mimic in RWPE-2 human prostate adenocarcinoma cells. Antioxid Redox Signal 2004;6:513-522.
62. Toh Y, Kuninaka S, Mori M, Oshiro T, Ikeda Y, Nakashima H, Baba H, Kohnoe S, Okamura T, Sugimachi K: Reduced expression of manganese superoxide dismutase mRNA may correlate with invasiveness in esophageal carcinoma. Oncology 2000;59:233-238.
63. Portakal O, Ozkaya O, Erden Inal M, Bozan B, Kosan M, Sayek I: Coenzyme Q10 concentrations and antioxidant status in tissues of breast cancer patients. Clin Biochem 2000;33:279-284.
64. Takada Y, Hachiya M, Park SH, Osawa Y, Ozawa T, Akashi M: Role of reactive oxygen species in cells overexpressing manganese superoxide dismutase: Mechanism for induction of radioresistance. Mol Cancer Res 2002;1:137-146.
65. Forsberg L, de Faire U, Morgenstern R: Oxidative stress, human genetic variation, and disease. Arch Biochem Biophys 2001;389:84-93.
66. Weydert C, Roling B, Liu J, Hinkhouse MM, Ritchie JM, Oberley LW, Cullen JJ: Suppression of the malignant phenotype in human pancreatic cancer cells by the overexpression of manganese superoxide dismutase. Mol Cancer Ther 2003;2:361-369.
67. Liu R, Oberley TD, Oberley LW: Transfection and expression of MnSOD cDNA decreases tumor malignancy of human oral squamous carcinoma SCC-25 cells. Hum Gene Ther 1997;8:585-595.