P-glycoprotein mediates celecoxib-induced apoptosis in multiple drug-resistant cell lines

Cancer Research

Volumn 67, Issue 10, 2007, Pages 4915-4923

  Fantappiè, Ornella ^a   Solazzo, Michela ^a   Lasagna, Nadia ^a   Platini, Francesca ^b   Tessitore, Luciana ^b   Mazzanti, Roberto ^a,c  

^a UNIVERSITY OF FLORENCE   (Italy)

^b UNIVERSITY OF EASTERN PIEDMONT   (Italy)

^c CAREGGI UNIVERSITY HOSPITAL   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE 3; CELECOXIB; CYCLOOXYGENASE 2; CYTOCHROME C; GLYCOPROTEIN P; MULTIDRUG RESISTANCE PROTEIN 1; PROTEIN BCL 2; PROTEIN BCL XL; SMALL INTERFERING RNA;

APOPTOSIS; ARTICLE; CELL COUNT; CONTROLLED STUDY; CYTOSOL; DRUG EFFECT; ENZYME ACTIVATION; GENE TRANSLOCATION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; LIVER CELL CARCINOMA; MITOCHONDRION; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ANIMALS; APOPTOSIS; BCL-2-ASSOCIATED X PROTEIN; BCL-X PROTEIN; CARCINOMA, HEPATOCELLULAR; CELL LINE, TUMOR; CYCLOOXYGENASE 2; CYTOCHROMES C; DRUG RESISTANCE, MULTIPLE; HT29 CELLS; HUMANS; LIVER NEOPLASMS; MICE; MITOCHONDRIA; NIH 3T3 CELLS; P-GLYCOPROTEIN; PROTO-ONCOGENE PROTEINS C-BCL-2; PYRAZOLES; SULFONAMIDES;

EID: 34250365663     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-06-3952     Document Type: Article

References (50)

1. Endicott JA, Ling V. The biochemistry of P-glycoprotein-mediated multidrug resistance. Annu Rev Biochem 1989;58:137-71.
2. Gottesman MM, Ling V. The molecular basis of multidrug resistance in cancer: the early years of P-giycoprotein research. FEBS Lett 2006;580:998-1009.
3. Mazzanti R, Croop JM, Gatmaitan Z, et al. Benzquinamide inhibits P-glycoprotein mediated drug efflux and potentiates anticancer agent cytotoxicity in multi-drug resistant cells. Oncol Res 1992;4:359-65.
4. Koga H, Sakisaka S, Ohishi M, et al. Expression of cyciooxygenase-2 in human hepatocellular carcinoma: relevance to tumor dedifferentiation. Hepatology 1999:29:688-96.
5. Smith WL, Garavito RM, DeWitt DL. Prostaglandin endoperoxide H synthases (cyclooxygenases)-1 and -2. J Biol Chem 1996;27:33157-60.
6. Eberhart CE, Dubois RN. Eicosanoids and the gastrointestinal tract. Gastroenterology 1995;109:285-301.
7. O'Neill GP, Ford-Hutchinson AW. Expression of mRNA for cyclooxygenase-1 and cyclooxygenase-2 in human tissues. FEBS Lett 1993;330:156-60.
8. Fosslien E. Biochemistry of cyclooxygenase (COX)-2 inhibitors and molecular pathology of COX-2 in neoplasia. Crit Rev Clin Lab Sci 2000;37:431-502.
9. Dubois RN, Abramson SB, Crofford L, et al. Cyclo-oxygenase in biology and disease. FASEB J 1998;12:1063-73.
10. McAdam BF, Mardini IA, Habib A, et al. Effect of regulated expression of human cyclooxygenase isoforms on eicosanoid and isoeicosanoid production in inflammation. J Clin Invest 2000;105:1473-82.
11. Murata H, Tsuji S, Tsujii M, et al. Promoter hypermethylation silences cyclooxygenase-2 (Cox-2) and regulates growth of human hepatocellular carcinoma cells. Lab Invest 2004;84:1050-9.
12. McGinty A, Chang YW, Sorokin A, Bokemeyer D, Dunn MJ. Cyclooxygenase-2 expression inhibits trophic withdrawal apoptosis in nerve growth factor-differentiated PC12 cells. J Biol Chem 2000;275:12095-101.
13. Trifan OC, Hla T. Cyclooxygenase-2 modulates cellular growth and promotes tumorigenesis. J Cell Mol Med 2003;7:207-22.
14. Cianchi F, Cortesini C, Fantappiè O, et al. Cyclo-oxygenase-2 activation mediates the proangiogenic effect of nitric oxide in colorectal cancer. Clin Cancer Res 2004;10:2694-704.
15. Nakano A, Watanabe N, Nishizaki Y, Takashimizu S, Matsuzaki S. Immunohistochemical studies on the expression of P-glycoprotein and p53 in relation to histological differentiation and cell proliferation in hepatocellular carcinoma. Hepatol Res 2003;25:158-65.
16. Fantappiè O, Masini E, Sardi I, et al. The MDR phenotype is associated with the expression of COX-2 and iNOS in a human hepatocellular carcinoma cell line. Hepatology 2002;35:843-52.
17. Lasagna N, Fantappiè O, Solazzo M, et al. Hepatocyte growth factor and inducible nitric oxide synthase are involved in multidrug resistance-induced angiogenesis in hepatocellular carcinoma cell lines. Cancer Res 2006;66:2673-82.
18. Patel VA, Dunn MJ, Sorokin A. Regulation of MDR-1 (P-glycoprotein) by cyclooxygenase-2. J Biol Chem 2002;277:38915-20.
19. Ziemann C, Schafer D, Rudell G, Kahl GF, Hirsch-Ernst Kl. The cyclooxygenase system participates in functional mdrlb overexpression in primary rat hepatocyte cultures. Hepatology 2002;35:579-88.
20. Sorokin A. Cyclooxygenase-2: potential role in regulation of drug efflux and multidrug resistance phenotype. Curr Pharm Des 2004;10:647-57.
21. Surowiak P, Materna V, Denkert C, et al. Significance of cyclooxygenase 2 and MDR1/P-glycoprotein coexpression in ovarian cancers. Cancer Lett 2006;235:272-80.
22. Johnstone RW, Cretney E, Smyth MJ. P-glycoprotein protects leukemia cells against caspase-dependent, but not caspase-independent, cell death. Blood 1999;93:1075-85.
23. Kojima H, Endo K, Moriyama H, et al. Abrogation of mitochondrial cytochrome c release and caspase-3 activation in acquired multidrug resistance. J Biol Chem 1998;273:16647-50.
24. Shimizu S, Konishi A, Kodama T, Tsujimoto Y. BH4 domain of antiapoptotic Bcl-2 family members closes voltage-dependent anion channel and inhibits apoptotic mitochondrial changes and cell death. Proc Natl Acad Sci U S A 2000;97:3100-5.
25. Jang MH, Jun do Y, Rue SW, Han K, Park W, Kim YH. Arginine antimetabolite L-canavanine induces apoptotic cell death in human Jurkat T cells via caspase-3 activation regulated by Bcl-2 or Bcl-xL. Biochem Biophys Res Commun 2002;295:283-8.
26. Takahashi M, Saito H, Atsukawa K, Ebinuma H, Okuyama T, Ishii II. Bcl-2 prevents doxorubicin-induced apoptosis of human liver cancer cells. Hepatol Res 2003;25:192-201.
27. Meric JB, Rottey S, Olaussen K, et al. Cyclooxygenase-2 as a target for anticancer drug development. Crit Rev Oncol Hematol 2006;59:51-64.
28. Wu T. Cyclooxygenase-2 in hepatocellular carcinoma. Cancer Treat Rev 2006;32:28-44.
29. Leng J, Han C, Demetris AJ, Michalopoulos GK, Wu T. Cyclooxygenase-2 promotes hepatocellular carcinoma cell growth through Akt activation: evidence for Akt inhibition in celecoxib-induced apoptosis. Hepatology 2003;38:756-68.
30. Fodera D, D'Alessandro N, Cusimano A, et al. Induction of apoptosis and inhibition of cell growth in human hepatocellular carcinoma cells by COX-2 inhibitors. Ann N Y Acad Sci 2004;1028:440-9.
31. Grosch S, Tegeder I, Niederberger E, Brautigam L, Geisslinger G. COX-2 independent induction of cell cycle arrest and apoptosis in colon cancer cells by the selective COX-2 inhibitor celecoxib. FASEB J 2001;15:2742-4.
32. Rahman MA, Dhar DK, Yamaguchi E, et al. Coexpression of inducible nitric oxide synthase and COX-2 in hepatocellular carcinoma and surrounding liver: possible involvement of COX-2 in the angiogenesis of hepatitis C virus-positive cases. Clin Cancer Res 2001;7:1325-32.
33. Cui W, Yu CH, Hu KQ. In vitro and in vivo effects and mechanisms of celecoxib-induced growth inhibition of human hepatocellular carcinoma cells. Clin Cancer Res 2005;11:8213-21.
34. MacNab GM, Alexander JJ, Lecatsas G, Bey EM, Urbanowicz JM. Hepatitis B surface antigen produced by a human hepatoma cell line. Br J Cancer 1976;34:509-15.
35. Riganti C, Miraglia E. Viarisio D, et al. Nitric oxide reverts the resistance to doxorubicin in human colon cancer cells by inhibiting the drug efflux. Cancer Res 2005;65:516-25.
36. Brandon EF, Bosch TM, Deenen MJ, et al. Validation of in vitro cell models used in drug metabolism and transport studies; genotyping of cytochrome P450, phase II enzymes and drug transporter polymorphisms in the human hepatoma (HepG2), ovarian carcinoma (IGROV-1) and colon carcinoma (CaCo-2, LS180) cell lines. Toxicol Appl Pharmacol 2006;211:1-10.
37. Solazzo M, Fantappiè O, Lasagna N, Sassoli C, Nosi D, Mazzanti R. P-gp localization in mitochondria and its functional characterization in multiple drug-resistant cell lines. Exp Cell Res 2006;312:4070-8.
38. Maier TJ, Janssen A, Schmidt R, Geisslinger G, Grosch S. Targeting the β-catenin/APC pathway: a novel mechanism to explain the cyclooxygenase-2-independent anticarcinogenic effects of celecoxib in human colon carcinoma cells. FASEB J 2005;19:1353-5.
39. Wu H, Hait WN, Yang JM. Small interfering RNA-induced suppression of MDR1 (P-glycoprotein) restores sensitivity to multidrug-resistant cancer cells. Cancer Res 2003;63:1515-9.
40. Mazzanti R, Fantappiè O, Kamimoto Y, Gatmaitan Z, Gentilini P, Arias IM. Bile acid inhibition of P-glycoprotein-mediated transport in multidrug-resistant cells and rat liver canalicular membrane vesicles. Hepatology 1994;20:170-6.
41. Mazzanti R, Fantappiè O, Fabrizio P, Relli P. Susceptibility to lipid peroxidation of human hepatocellular carcinoma cell lines with different levels of multiple drug-resistant phenotype. Lab Invest 1995;73:419-23.
42. Breier A, Barancik M, Sulova Z, Uhrik B. P-glycoprotein-implications of metabolism of neoplastic cells and cancer therapy. Curr Cancer Drug Targets 2005;5:457-68.
43. Hashitani S, Urade M, Nishimura N, et al. Apoptosis induction and enhancement of cytotoxicity of anticancer drugs by celecoxib, a selective cyclooxygenase-2 inhibitor, in human head and neck carcinoma cell lines. Int J Oncol 2003;23:665-72.
44. Awara WM, El-Sisi AE, El-Sayad ME, Goda AE. The potential role of cyclooxygenase-2 inhibitors in the treatment of experimentally-induced mammary tumour: does celecoxib enhance the anti-tumour activity of doxorubicin? Pharmacol Res 2004;50:487-98.
45. Dvory-Sobol H, Cohen-Noyman E, Kazanov D, et al. Celecoxib leads to G2/M arrest by induction of p21 and down-regulation of cyclin B1 expression in a p53-independent manner. Eur J Cancer 2006;42:422-6.
46. Gierse JK, Koboldt CM, Walker MC, Seibert K, Isakson PC. Kinetic basis for selective inhibition of cyclooxygenases. Biochem J 1999;339:607-14.
47. Li CQ, Wogan GN. Nitric oxide as a modulator of apoptosis. Cancer Lett 2005;226:1-15.
48. Kern MA, Haugg AM, Koch AF, et al. Cyclooxygenase-2 inhibition induces apoptosis signaling via death receptors and mitochondria in hepatocellular carcinoma. Cancer Res 2006;66:7059-66.
49. Zhang Z, Lai GH, Sirica AE. Celecoxib-induced apoptosis in rat cholangiocarcinoma cells mediated by Akt inactivation and Bax translocation. Hepatology 2004;39:1028-37.
50. Mantovani I, Cappellini A, Tazzari PL, Papa V, Cocco L, Martelli AM. Caspase-dependent cleavage of 170-kDa P-glycoprotein during apoptosis of human T-lympho-blastoid CEM cells. J Cell Physiol 2006;207:836-44.