P-glycoprotein depresses cisplatin sensitivity in L1210 cells by inhibiting cisplatin-induced caspase-3 activation

Toxicology in Vitro

Volumn 26, Issue 3, 2012, Pages 435-444

  Gibalová, Lenka ^a   Šereš, Mário ^a   Rusnák, Andrej ^a   Ditte, Peter ^b   Labudová, Martina ^b   Uhrík, Branislav ^a   Pastorek, Jaromir ^b   Sedlák, Ján ^c   Breier, Albert ^a   Sulová, Zdenka ^a  

^a INSTITUTE OF MOLECULAR PHYSIOLOGY AND GENETICS   (Slovakia)

^b INSTITUTE OF VIROLOGY   (Slovakia)

^c CANCER RESEARCH INSTITUTE   (Slovakia)

Author keywords

Apoptosis; Caspases; Cisplatin; Drug resistance; HSP90; Leukemia; P glycoprotein; P53; Proteins of Bcl 2 family

Indexed keywords

CASPASE 3; CISPLATIN; GLYCOPROTEIN P; HEAT SHOCK PROTEIN 90; PROTEIN BAX; PROTEIN BCL 2; PROTEIN P53;

APOPTOSIS; ARTICLE; CELL ULTRASTRUCTURE; CHEMOSENSITIVITY; CONTROLLED STUDY; DNA FRAGMENTATION; DRUG RESISTANCE; ENZYME INHIBITION; PROTEIN EXPRESSION; PROTEIN FUNCTION;

ANIMALS; ANTINEOPLASTIC AGENTS; APOPTOSIS; CASPASE 3; CISPLATIN; DNA FRAGMENTATION; DRUG RESISTANCE, NEOPLASM; HSP90 HEAT-SHOCK PROTEINS; HUMANS; LEUKEMIA L1210; MICE; P-GLYCOPROTEIN; TUMOR SUPPRESSOR PROTEIN P53; UP-REGULATION; VERAPAMIL; VINCRISTINE;

EID: 84857686976     PISSN: 08872333     EISSN: 18793177     Source Type: Journal    
DOI: 10.1016/j.tiv.2012.01.014     Document Type: Article

References (50)

1. Baguley B.C. Multidrug resistance in cancer. Methods Mol. Biol. 2010, 596:1-14.
2. Bauer J.A., Kumar B., Cordell K.G., Prince M.E., Tran H.H., Wolf G.T., Chepeha D.B., Teknos T.N., Wang S., Eisbruch A., Tsien C.I., Urba S.G., Worden F.P., Lee J., Griffith K.A., Taylor J.M., D'Silva N., Wang S.J., Wolter K.G., Henson B., Fisher S.G., Carey T.E., Bradford C.R. Targeting apoptosis to overcome cisplatin resistance: a translational study in head and neck cancer. Int. J. Radiat. Oncol. Biol. Phys. 2007, 69(2 Suppl.):S106-S108.
3. Bear C.E. Drugs transported by P-glycoprotein inhibit a 40pS outwardly rectifying chloride channel. Biochem. Biophys. Res. Commun. 1994, 200(1):513-521.
4. Beretta G.L., Righetti S.C., Lombardi L., Zunino F., Perego P. Electron microscopy analysis of early localization of cisplatin in ovarian carcinoma cells. Ultrastruct. Pathol. 2002, 26(5):331-334.
5. Bitomsky N., Hofmann T.G. Apoptosis and autophagy: regulation of apoptosis by DNA damage signalling - roles of p53, p73 and HIPK2. FEBS J. 2009, 276(21):6074-6083.
6. 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(6):457-468.
7. Broxterman H.J., Gotink K.J., Verheul H.M. Understanding the causes of multidrug resistance in cancer: a comparison of doxorubicin and sunitinib. Drug Resist. Updat. 2009, 12(4-5):114-126.
8. Brunelle J.K., Letai A. Control of mitochondrial apoptosis by the Bcl-2 family. J. Cell Sci. 2009, 122(Pt 4):437-441.
9. Campos L., Oriol P., Sabido O., Guyotat D. Simultaneous expression of P-glycoprotein and BCL-2 in acute myeloid leukemia blast cells. Leuk. Lymphoma 1997, 27(1-2):119-125.
10. Degli Esposti M., Dive C. Mitochondrial membrane permeabilisation by Bax/Bak. Biochem. Biophys. Res. Commun. 2003, 304(3):455-461.
11. Del Principe M.I., Del Poeta G., Maurillo L., Buccisano F., Venditti A., Tamburini A., Bruno A., Cox M.C., Suppo G., Tendas A., Gianni L., Postorino M., Masi M., Del Principe D., Amadori S. P-glycoprotein and BCL-2 levels predict outcome in adult acute lymphoblastic leukaemia. Br. J. Haematol. 2003, 121(5):730-738.
12. Demeule M., Brossard M., Beliveau R. Cisplatin induces renal expression of P-glycoprotein and canalicular multispecific organic anion transporter. Am. J. Physiol. 1999, 277(6 Pt 2):F832-F840.
13. Fairchild C.R., Moscow J.A., O'Brien E.E., Cowan K.H. Multidrug resistance in cells transfected with human genes encoding a variant P-glycoprotein and glutathione S-transferase-pi. Mol. Pharmacol. 1990, 37(6):801-809.
14. Gerlier D., Thomasset N. Use of MTT colorimetric assay to measure cell activation. J. Immunol. Methods 1986, 94(1-2):57-63.
15. Gibalova L., Sedlak J., Labudova M., Barancik M., Rehakova A., Breier A., Sulova Z. Multidrug resistant P-glycoprotein positive L1210/VCR cells are also cross-resistant to cisplatin via a mechanism distinct from P-glycoprotein-mediated drug efflux activity. Gen. Physiol. Biophys. 2009, 28(4):391-403.
16. Hamaguchi K., Godwin A.K., Yakushiji M., O'Dwyer P.J., Ozols R.F., Hamilton T.C. Cross-resistance to diverse drugs is associated with primary cisplatin resistance in ovarian cancer cell lines. Cancer Res. 1993, 53(21):5225-5232.
17. Hoffman M.M., Wei L.Y., Roepe P.D. Are altered pHi and membrane potential in hu MDR 1 transfectants sufficient to cause MDR protein-mediated multidrug resistance?. J. Gen. Physiol. 1996, 108(4):295-313.
18. Homolya L., Varadi A., Sarkadi B. Multidrug resistance-associated proteins: export pumps for conjugates with glutathione, glucuronate or sulfate. BioFactors 2003, 17(1-4):103-114.
19. Chipuk J.E., Green D.R. Dissecting p53-dependent apoptosis. Cell Death Differ. 2006, 13(6):994-1002.
20. Idriss H.T., Hannun Y.A., Boulpaep E., Basavappa S. Regulation of volume-activated chloride channels by P-glycoprotein: phosphorylation has the final say!. J. Physiol. 2000, 524(Pt 3):629-636.
21. Kirsch D.G., Doseff A., Chau B.N., Lim D.S., de Souza-Pinto N.C., Hansford R., Kastan M.B., Lazebnik Y.A., Hardwick J.M. Caspase-3-dependent cleavage of Bcl-2 promotes release of cytochrome c. J. Biol. Chem. 1999, 274(30):21155-21161.
22. Krishan A., Dandekar P.D. DAPI fluorescence in nuclei isolated from tumors. J. Histochem. Cytochem. 2005, 53(8):1033-1036.
23. Laemmli U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970, 227(5259):680-685.
24. Lavie Y., Fiucci G., Czarny M., Liscovitch M. Changes in membrane microdomains and caveolae constituents in multidrug-resistant cancer cells. Lipids 1999, 34(Suppl):S57-63.
25. Lee J.T., Gu W. The multiple levels of regulation by p53 ubiquitination. Cell Death Differ. 2010, 17(1):86-92.
26. Lessene G., Czabotar P.E., Colman P.M. BCL-2 family antagonists for cancer therapy. Nat. Rev. Drug Discov. 2008, 7(12):989-1000.
27. Muller L., Schaupp A., Walerych D., Wegele H., Buchner J. Hsp90 regulates the activity of wild type p53 under physiological and elevated temperatures. J. Biol. Chem. 2004, 279(47):48846-48854.
28. Nagata S. Apoptotic DNA fragmentation. Exp. Cell Res. 2000, 256(1):12-18.
29. Olofsson M.H., Havelka A.M., Brnjic S., Shoshan M.C., Linder S. Charting calcium-regulated apoptosis pathways using chemical biology: role of calmodulin kinase II. BMC Chem. Biol 2008, 8:2.
30. Oltvai Z.N., Milliman C.L., Korsmeyer S.J. Bcl-2 heterodimerizes in vivo with a conserved homolog, Bax, that accelerates programmed cell death. Cell 1993, 74(4):609-619.
31. Pallis M., Russell N. Strategies for overcoming p-glycoprotein-mediated drug resistance in acute myeloblastic leukaemia. Leukemia 2004, 18(12):1927-1930.
32. Pallis M., Turzanski J., Higashi Y., Russell N. P-glycoprotein in acute myeloid leukaemia: therapeutic implications of its association with both a multidrug-resistant and an apoptosis-resistant phenotype. Leuk. Lymphoma 2002, 43(6):1221-1228.
33. Pastan I., Gottesman M.M., Ueda K., Lovelace E., Rutherford A.V., Willingham M.C. A retrovirus carrying an MDR1 cDNA confers multidrug resistance and polarized expression of P-glycoprotein in MDCK cells. Proc. Natl. Acad. Sci. USA 1988, 85(12):4486-4490.
34. Polekova L., Barancik M., Mrazova T., Pirker R., Wallner J., Sulova Z., Breier A. Adaptation of mouse leukemia cells L1210 to vincristine. Evidence for expression of P-glycoprotein. Neoplasma 1992, 39(2):73-77.
35. Ruefli A.A., Johnstone R.W. A role for P-glycoprotein in regulating cell growth and survival. Clin. Appl. Immunol. Rev. 2003, 4(1):31-41.
36. Seres M., Ditte P., Breier A., Sulova Z. Effect of thapsigargin on P-glycoprotein-negative and P-glycoprotein-positive L1210 mouse leukaemia cells. Gen. Physiol. Biophys. 2010, 29(4):396-401.
37. Smaili S., Hirata H., Ureshino R., Monteforte P.T., Morales A.P., Muler M.L., Terashima J., Oseki K., Rosenstock T.R., Lopes G.S., Bincoletto C. Calcium and cell death signaling in neurodegeneration and aging. An. Acad. Bras. Cienc. 2009, 81(3):467-475.
38. Sorenson C.M., Barry M.A., Eastman A. Analysis of events associated with cell cycle arrest at G2 phase and cell death induced by cisplatin. J. Natl Cancer Inst. 1990, 82(9):749-755.
39. Sulova Z., Ditte P., Kurucova T., Polakova E., Rogozanova K., Gibalova L., Seres M., Skvarkova L., Sedlak J., Pastorek J., Breier A. The presence of P-glycoprotein in L1210 cells directly induces down-regulation of cell surface saccharide targets of concanavalin A. Anticancer Res. 2010, 30(9):3661-3668.
40. Sulova Z., Mislovicova D., Gibalova L., Vajcnerova Z., Polakova E., Uhrik B., Tylkova L., Kovarova A., Sedlak J., Breier A. Vincristine-induced overexpression of P-glycoprotein in L1210 cells is associated with remodeling of cell surface saccharides. J. Proteome Res. 2009, 8(2):513-520.
41. Sulova Z., Orlicky J., Fiala R., Dovinova I., Uhrik B., Seres M., Gibalova L., Breier A. Expression of P-glycoprotein in L1210 cells is linked with rise in sensitivity to Ca2+. Biochem. Biophys. Res. Commun. 2005, 335(3):777-784.
42. Sulova, Z., Seres, M., Barancik, M., Gibalova, L., Uhrik, B., Polekova, L., Breier, A., 2009b. Does any relationship exist between P-glycoprotein-mediated multidrug resistance and intracellular calcium homeostasis?. Gen. Physiol. Biophys. 28 Spec No, Focus, F89-F95.
43. Towbin H., Staehelin T., Gordon J. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc. Natl. Acad. Sci. USA 1979, 76(9):4350-4354.
44. Uhrik B., El-Saggan A.H., Seres M., Gibalova L., Breier A., Sulova Z. Structural differences between sensitive and resistant L1210 cells. Gen. Physiol. Biophys. 2006, 25(4):427-438.
45. Uhrik B., Tribulova N., Klobusicka M., Barancik M., Breier A. Characterization of morphological and histochemical changes induced by overexpression of P-glycoprotein in mouse leukemic cell line L1210. Neoplasma 1994, 41(2):83-88.
46. Walerych D., Kudla G., Gutkowska M., Wawrzynow B., Muller L., King F.W., Helwak A., Boros J., Zylicz A., Zylicz M. Hsp90 chaperones wild-type p53 tumor suppressor protein. J. Biol. Chem. 2004, 279(47):48836-48845.
47. Wozniak K., Czechowska A., Blasiak J. Cisplatin-evoked DNA fragmentation in normal and cancer cells and its modulation by free radical scavengers and the tyrosine kinase inhibitor STI571. Chem. Biol. Interact. 2004, 147(3):309-318.
48. Xiao T., Choudhary S., Zhang W., Ansari N.H., Salahudeen A. Possible involvement of oxidative stress in cisplatin-induced apoptosis in LLC-PK1 cells. J. Toxicol. Environ. Health A 2003, 66(5):469-479.
49. Yang X., Page M. P-glycoprotein expression in ovarian cancer cell line following treatment with cisplatin. Oncol. Res. 1995, 7(12):619-624.
50. Youle R.J., Strasser A. The BCL-2 protein family: opposing activities that mediate cell death. Nat. Rev. Mol. Cell Biol. 2008, 9(1):47-59.